Constraints On Somatotopic Organization in The Primary Motor Cortex

INVITED REVIEW
Constraints on Somatotopic Organization in the Primary

Motor Cortex
MARC H. SCHIEBER
Departments of Neurology, Neurobiology and Anatomy, Brain and Cognitive Science, and Physical Medicine and
Rehabilitation, the Center for Visual Science, and the Brain Injury Rehabilitation Program at St. Mary’s Hospital,
University of Rochester School of Medicine and Dentistry, Rochester, New York 14642
Received 9 January 2001; accepted in final form 5 July 2001
Schieber, Marc H. Constraints on somatotopic organization in the of the canine cortex, one of the earliest demonstrations of a
Downloaded from http://jn.physiology.org/ by 10.220.33.6 on March 9, 2017

primary motor cortex. J Neurophysiol 86: 2125–2143, 2001. Since the specific function of a particular cortical region (Walshe 1948).
1870s, the primary motor cortex (M1) has been known to have a As techniques for electrical stimulation improved, increasingly
somatotopic organization, with different regions of cortex participat- detailed maps of body part representation in M1 became avail-
ing in control of face, arm, and leg movements. Through the middle
of the 20th century, it seemed possible that the principle of somato-
able, culminating in the well-known summary diagrams of
topic organization extended to the detailed representation of different Penfield’s homunculus (Penfield and Rasmussen 1950) and
body parts within each of the three major representations. The arm Woolsey’s simiusculus (Woolsey et al. 1952). These icons of
region of M1, for example, was thought to contain a well-ordered, neuroscience commonly are interpreted as showing a system-
point-to-point representation of the movements or muscles of the atic, spatially organized, point-to-point mapping of control of
thumb, index, middle, ring, and little fingers, the wrist, elbow, and different body parts by different pieces of M1 cortex (Schott
shoulder, as conveyed by the iconic homunculus and simiusculus. In 1993). Indeed, in its ultimate form, Penfield’s homunculus
the last quarter of the 20th century, however, experimental evidence included a line representing the mediolateral ribbon of M1,
has accumulated indicating that within-limb somatotopy in M1 is not broken into sequential line segments representing different
spatially discrete nor sequentially ordered. Rather, beneath gradual body parts, down to different segments for the thumb, index,
somatotopic gradients of representation, the representations of differ-
ent smaller body parts or muscles each are distributed widely within
middle, ring, and little fingers.
the face, arm, or leg representation, such that the representations of In the last quarter of the 20th century, however, experimen-
any two smaller parts overlap extensively. Appreciation of this un- tal evidence has accumulated indicating that the control of
derlying organization will be essential to further understanding of the different body parts from M1 is not nearly so somatotopically
contribution to control of movement made by M1. Because no single organized as the homunculus and simiusculus seem to suggest.
experiment disproves a well-ordered within-limb somatotopic organi- While it remains clear that the head, upper extremity, and
zation in M1, here I review the accumulated evidence, using a frame- lower extremity have sequential and largely separate represen-
work of six major features that constrain the somatotopic organization tations, the representations of smaller body parts are widely
of M1: convergence of output, divergence of output, horizontal inter- distributed within these major regions. In retrospect, data ob-
connections, distributed activation, effects of lesions, and ability to tained from the 1870s to the present can be seen to be consis-
reorganize. Review of the classic experiments that led to development
of the homunculus and simiusculus shows that these data too were
tent with this distributed organization as well. Consequently,
consistent with distributed within-limb somatotopy. I conclude with the territory controlling one body part overlaps extensively
speculations on what the constrained somatotopy of M1 might tell us with the territory controlling adjacent body parts. For example,
about its contribution to control of movement. the M1 territory controlling the thumb overlaps extensively
with the territories controlling the fingers.
Here I review this evidence in a framework of six factors
INTRODUCTION that constrain the somatotopic organization of M1. 1) Conver-
gent output from a large M1 territory controls any particular
Somatotopic organization long has been the hallmark of the body part, joint or muscle. 2) Divergent output of many single
primary motor cortex (M1). The concept of a cortical region M1 neurons reaches multiple spinal motoneuron pools. 3)
systematically organized to control movements of different Horizontal connections interlink the cortex throughout a major
body parts was first hypothesized by Hughlings Jackson in the body part region. 4) Widely distributed activity appears in a
1870s, based on his observations of certain epileptic patients in major body part region whenever any smaller body part is
whom convulsive movements systematically marched from moved. 5) Partial inactivation of a major region affects mul-
one part of the body to adjacent parts (Jackson 1958). The tiple smaller body parts simultaneously. 6) Plasticity limits the
existence of such a cortical region was demonstrated contem- degree to which control of a specific body part can be assigned
poraneously by Fritsch and Hitzig using electrical stimulation to a particular piece of cortex. Although I will deal mainly with
Address for reprint requests: University of Rochester Medical Center, Dept. The costs of publication of this article were defrayed in part by the payment
of Neurology, 601 Elmwood Ave., Box 673, Rochester, NY 14642 (E-mail: of page charges. The article must therefore be hereby marked ‘‘advertisement’’
mhs@cvs.rochester.edu). in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
www.jn.org 0022-3077/01 $5.00 Copyright © 2001 The American Physiological Society 2125
2126 M. H. SCHIEBER
the upper extremity region (from which the most experimental Classical studies employing stimulation of the cortical
evidence is available), these six factors appear to apply as well surface
to the representations of the face and lower extremity. No one
factor alone unequivocally disproves a detailed within-limb Because the classical studies that employed stimulation of
somatotopy, nor can any single experiment. Yet considered the cortical surface commonly are assumed to have demon-
altogether, they compel us to conclude that control of each part strated a detailed within-limb somatotopic organization, I be-
of the upper limb, lower limb, or face is widely distributed gin by reviewing exactly what was demonstrated in these
within the overall representation. To progress in understanding studies. By modern standards, the electrical stimuli employed
M1’s contribution to motor control, we must consider the in these studies were intense and prolonged, exciting relatively
implications of these constraints on the somatotopic organiza- large regions of cortex, and evoked overt movements rather
tion of M1. than the brief flicks and twitches evoked by ICMS. Penfield
and Boldrey (1937) published a map of 77 precentral locations
CONVERGENCE from which cortical surface stimulation elicited movements of
the different digits of the hand in studies of 126 human subjects
Outputs from large territories of M1 converge on the spinal (Fig. 1A). The overall region from which stimulation produced
motoneuron pool of any given muscle. The cortical territory for finger movements extended 55 mm along the central sulcus.
each muscle is so large as to preclude spatially separate terri- Inspection of their figure shows that thumb movements were

tories for each muscle. Instead, the M1 territories from which elicited at both the lateral and medial limits of this region, as
outputs converge on two upper extremity muscles overlap were movements of the little finger, and of the other digits as
extensively. This principle of convergence was articulated well. Furthermore, comparing the region from which finger
most precisely by the work of Charles Phillips and his collab- movements were evoked with the region from which arm
orators (described in the following sub-sections), but all studies movements were evoked showed large, extensively overlap-
of movements evoked by stimulation of M1 have been consis- ping territories representing different proximodistal parts of the
tent with such convergence and overlap, from the classical upper extremity (Fig. 1B).
studies with cortical surface stimulation that led to the homun- Because data from multiple subjects were compiled in these
culus and simiusculus, to more recent studies using intracorti- maps, inter-individual variation might have accounted for the
cal microstimulation (ICMS). large and overlapping territories of different digits and more
FIG. 1. Convergence and overlap in Penfield’s data. Enlargements are shown from Figs. 12A and 25B of Penfield and Boldrey
(1937). The region enlarged is indicated by the rectangle drawn on the inset taken from their standardized map of the hemisphere,
but note that whereas the region shown in B extends laterally to the Sylvian fissure and therefore includes the face representation,
the region shown in A does not. A: locations from which finger movements were elicited in data compiled from 126 patients. If only
certain digits moved, they are indicated with Roman numerals: I ⫽ thumb through V ⫽ little finger. Black dots indicate locations
where stimulation elicited movement of all the digits. Note that, contrary to the discrete order implied by the homunculus, thumb
movements were elicited medially as well as laterally, and little finger movements were elicited laterally as well as medially. B:
outlines encompass the total territory from which movements of the fingers (E E E), entire hand (¦ ¦ ¦), or more proximal arm
(⫹ – ⫹ – ⫹) were evoked. Note the overlap of distal and proximal representations. (Reproduced with permission of the Literary
Executors of Wilder Penfield)
J Neurophysiol • VOL 86 • NOVEMBER 2001 • www.jn.org

CONSTRAINTS ON SOMATOTOPY IN M1 2127
proximal parts of the upper extremity. In single subjects, an well (points marked by upside-down L, N, M). Finger move-
orderly, segregated somatotopic arrangement might have been ments were elicited from two more medial points as well (Z
apparent. Inspection of records from single patients reveals, and O), with the most medial of these (O) surrounded by other
however, that such was not the case. Figure 2 shows, for points from which more proximal arm movements were
example, detailed results of intraoperative stimulation in one evoked (7, R, X). Thus a well-ordered somatotopic represen-
patient studied by Penfield and colleagues. Although an overall tation of the upper extremity was not evident in the details of
somatotopic trend was apparent in this single case, with move- single cases such as this.
ments of the digits being evoked more often laterally along the Penfield and Rasmussen (1950, p. 56), commenting on their
Rolandic fissure and movements of more proximal parts of the homunculus, noted: “A figurine of this sort cannot give an
upper extremity being evoked more often medially, move- accurate indication of the specific joints in which movement
ments of different parts were not elicited from discrete loca- takes place, for in most cases movement appears at more than
tions arrayed in simple somatotopic order. The thumb, for one joint simultaneously. . . . The motor homunculus may be
example, was involved in the movements produced by stimu- used as an aid to memory in regard to movement sequence and
lation at three points along the central sulcus, and at each of the relative extent of cortex in which such movement finds
these points stimulation evoked movements of other digits as representation. It is a cartoon of representation in which sci-

FIG. 2. Details of intraoperative stimulation in an individual human patient. The sketch reproduced here from case records
shows the borders of the craniotomy (cross-hatching) and locations of paper markers placed at stimulated locations (upside-down
letters and numbers), both drawn by Penfield and colleagues on their standard map of the hemispheric surface based on their
intraoperative photograph. To this reproduced sketch, I have added selected details from the transcribed intraoperative notes
recording the results of stimulation at each location, linked to each marker by a straight line. No response to stimulation was
obtained at point B, 10, or 11; and no transcribed note was available for point H or 2. Note that, although movements of the digits
were generally obtained laterally and more proximal movements medially, movements of different digits or more proximal parts
of the extremity were not obtained from separate, somatotopically ordered points. This particular case was chosen here because of
the relatively large number of points stimulated along the precentral gyrus (in many other cases, because of the possible risk of
setting off seizures by stimulation of the motor cortex, many points along the postcentral gyrus were stimulated, and only a few
along the precentral gyrus; personal communication, Dr. William Feindel), and because no cortical lesion was evident at surgery.
The only lesion found was a meningeal cicatrix close to the midline (in the sketch reproduced here, the wandering dashed line close
to the midline delimited a territory of “whitening of the arachnoid”). Although a detailed description of the patient’s typical seizures
was not available, he had “Jacksonian epilepsy” with an epigastric aura. This patient (MO) was described by Penfield and
Rasmussen (1950, their Fig. 32) in reference to eye turning. Transcribed operative notes, an intraoperative photograph of the brain
with paper markers placed on the cortical surface, and the sketch reproduced here, all were provided courtesy of the Penfield
Archive (Montreal Neurological Institute, Dr. William Feindel, Curator).

2128 M. H. SCHIEBER
entific accuracy is impossible.” Although the overlapping rep- motor simiusculi (their Fig. 131), Woolsey and colleagues
resentations of adjacent body parts observed by Penfield and wrote, “It must be emphasized . . . that this diagram is an
colleagues might have resulted from current spread across an inadequate representation of the localization pattern, since in a
underlying discrete and orderly somatotopic representation, the line drawing one cannot indicate the successive overlap which
overlap also could have been a genuine feature of the under- is so characteristic a feature of cortical representation. . . .”
lying representation in M1. (Woolsey et al. 1952, p. 252).
The detailed results of similar studies on a rhesus monkey While the examples illustrated above come from the work of
and on a human from the work of Woolsey and colleagues are Penfield’s group and Woolsey’s group, similar evidence con-
illustrated in Fig. 3. In both species, evoked movements typi- sistent with convergence and overlap was present in the de-
cally involved more than one digit and/or more proximal joint. tailed results of other investigators who employed cortical
In both species, movements involving the thumb were elicited surface stimulation in systematic exploration of M1. The num-
by stimuli delivered at different locations scattered over much ber of such studies is too large for each to be mentioned here,
of the upper extremity representation. Similarly, stimulation at but some additional examples may illustrate two general fea-
many different locations elicited movements involving the tures of this literature. First, the impression of discrete soma-
little finger. Although the thumb appears more heavily repre- totopic order versus convergence and overlap varied with the
sented in the lateral aspect of the upper extremity representa- number of points stimulated. Stimulating a limited number of
tion and the little finger appears more heavily represented widely spaced points along the central sulcus often demon-

medially, the territory in which evoked movements involved strated a progression from shoulder movements medially to
the thumb overlaps considerably with the territory in which finger and thumb movements laterally (Bucy 1949; Fulton and
evoked movements involved the little finger. As with Pen- Keller 1932). Even in these studies, however, some points
field’s studies, given the possible spread of stimulating current, failed to follow a strict somatotopic order. In studies sampling
Woolsey’s data would be consistent either with discrete, so- a larger number of points, convergence and overlap became
matotopically segregated representations of the thumb and more apparent. In studies of anthropoid apes, for example,
little finger, or with overlapping representations in which out- Leyton and Sherrington (1917) stimulated a relatively large
puts to the muscles serving each digit converge from large number of points in each animal studied, and listed 135 dif-
cortical territories. The same argument would apply to other ferent combinations of primary, secondary, tertiary, and qua-
pairings of digits, or pairings of digit and wrist, wrist and ternary evoked upper extremity movements; these studies show
elbow, and elbow and shoulder. In the text bracketing the considerable overlap of the representation of different joints
FIG. 3. Convergence and overlap in Woolsey’s data. Maps of evoked movements obtained by Woolsey and colleagues (A) in
a monkey (Macaca irus) (Woolsey et al. 1952), and (B) in a human (Woolsey et al. 1979). Inset figures of an entire brain indicate
the areas enlarged. In A, dashed lines indicate areas in the anterior bank of the central sulcus (right) and posterior bank of the arcuate
sulcus (left) exposed for stimulation. In both A and B, figurines show which parts of the body moved on stimulation at each location,
with black shading indicating the most vigorous, cross-hatching intermediate and stippling the least movement. In both species, the
territories from which movements of the thumb and different fingers were evoked were large and extensively overlapping.
(Modified from Schieber 1990)

and movements. Here, then, is a second general feature: focus- 1965). At threshold for direct activation of corticospinal neu-
ing on only the initial or most prominent elicited movement rons, then, more superficial cortical interneurons were excited
was more revealing of somatotopic order, whereas attending to as well. These interneurons could excite corticospinal neurons
all the movements elicited by stimulation at each point sug- not only directly beneath the stimulating electrode, but also
gested more extensive convergence and overlap (Beevor and lateral to the electrode (see Horizontal interconnections, be-
Horsley 1887; Ferrier 1873; Hines 1940; Murphy and Gellhorn low). Horizontal spread through transynaptic excitation of cor-
1945). For example, by focusing only on the primary move- ticospinal neurons might artifactually enlarge the cortical ter-
ment evoked by stimulation at each site, and comparing non- ritories from which a given movement was evoked, producing
adjacent joints (e.g., shoulder vs. fingers), Leyton and Sher- even more overlap. To limit such horizontal spread of excita-
rington demonstrated a gradual somatotopic progression tion, vertical incisions in the cortex could be made to isolate
consistent with the homunculus and simiusculus (e.g., their small (3 ⫻ 5 mm) islands of cortex; however, this experimental
Figs. 16 and 17), even though their data are consistent with manipulation failed to eliminate the extensively overlapping
extensive overlap when all movements of all joints were con- territories (Murphy and Gellhorn 1945).
sidered. Nevertheless, it remained possible that if only a few, closely
Studies in which muscle contraction was measured during packed corticospinal neurons could be excited directly, the
cortical surface stimulation, instead of observing evoked map of evoked movements would resolve into discrete territo-
movement, also were consistent with convergence and overlap. ries for different movements or muscles. This possibility di-
Recording the tension developed by a number of monkey minished, however, when Phillips and co-workers found that

hindlimb muscles, for example, revealed that cortical surface brief (0.2-ms) low-amplitude, surface-anodal stimuli directly
stimulation only occasionally evoked contraction of one of the excited corticospinal neurons without indirect excitation (Hern
recorded muscles alone; much more often, multiple muscles et al. 1962). Recording intracellularly from baboon cervical
contracted simultaneously, although the cortical locations from motoneurons, and accounting for current spread in the cortex,
which maximal contraction was evoked differed from muscle they used such stimuli to demonstrate that the colony of cor-
to muscle (Chang et al. 1947). Similar results in humans have ticospinal neurons projecting monosynaptically to a single
been obtained in recent years by recording compound muscle cervical motoneuron must, in many instances, be spread over a
actions potentials in response to transcranial magnetic stimu- cortical territory of at least several square millimeters (the
lation (Krings et al. 1998; Wassermann et al. 1992). largest minimal territory they measured covered 20 mm2)
(Landgren et al. 1962). Moreover, the minimal territories con-
Were convergence and overlap artifactual? taining corticospinal neurons projecting to radial, ulnar, or
median nerve motoneurons (i.e., innervating different muscles)
Until the 1970s, much if not all of this evidence of conver- often overlapped. Thus even single motoneurons were shown
gence from large and overlapping territories moving different to receive converging input from relatively large cortical ter-
body parts could have been attributed to the spread of stimulus ritories, which overlap with the territories providing input to
effects, for two reasons. First, relatively large stimulating cur- motoneurons of other muscles.
rents (on the order of 0.5–1.5 mA) had to be used at the cortical
surface to evoke movements; in comparison, currents an order Studies employing ICMS
of magnitude smaller evoked movements when applied to a
peripheral nerve. The large currents applied to a point at the In the late 1960s and early 1970s, Asanuma and colleagues
cortical surface inevitably spread through a considerable vol- developed the technique of ICMS. Rather than stimulating with
ume of tissue. At threshold for evoking simple flick move- a large electrode touching the pial surface of the cortex, a
ments (e.g., 10-ms pulses of 0.5–1.5 mA), for example, surface microelectrode was advanced into the M1 cortex and posi-
stimulation evoked repetitive discharge in Betz cells up to 4 tioned close to layer V. Here, 0.2-ms pulses of only a few
mm horizontally distant from the surface point stimulated microamperes, delivered in trains of 10 –12 pulses at approx-
(Phillips 1956; see also Asanuma et al. 1976; Jankowska et al. imately 300 Hz, could evoke visible movement or recordable
1975a). Direct excitation of corticospinal neurons by surface electromyographic (EMG) activity. Single 10-␮A, 0.2-ms
stimulation thus occurred within a rather large area around the cathodal current pulses delivered in layer V were estimated to
stimulated point, but even a 4-mm horizontal spread of direct directly excite neuronal somata within a radius of only 88 ␮m,
Betz cell excitation could not account for the observed overlap which in cat anterior sigmoid gyrus would encompass only
of up to 55 mm. about 28 pyramidal neurons (Stoney et al. 1968). Initial studies
Second, corticospinal neurons at an even greater horizontal with ICMS indicated that a particular movement of a part of the
distance in theory could be excited indirectly. Single electrical forelimb, or contraction of a particular muscle, was evoked by
stimuli delivered at the cortical surface evoked multiple de- threshold ICMS applied within a small columnar zone of
scending volleys in the corticospinal tract. The earliest volley approximately 0.5–1 mm radius (Asanuma and Rosen 1972).
(D-wave) was produced by direct excitation of corticospinal Multiple small efferent zones scattered in the overall forelimb
neurons; later descending volleys (I-waves) resulted from ex- representation could be found for the same movement or mus-
citation of intracortical neurons which indirectly (trans-synap- cle. Discrete efferent zones representing different movements
tically) excited the corticospinal neurons (Patton and Amassian or muscles appeared intermingled like the different colors of
1954). D-waves were evoked by current spread from the point tiles in a mosaic.
of surface stimulation through the superficial cortical layers, The initial report of Asanuma and Rosen (1972) showed this
exciting the corticospinal neuron somata in layer V (Patton and mosaic arrangement by superimposing data from 10 Cebus
Amassian 1954), or their axons still deeper (Landau et al. monkeys (their Fig. 8). Subsequent studies from numerous

2130 M. H. SCHIEBER
laboratories in many species, including detailed studies of stimulation at several sites scattered in the forelimb represen-
single subjects, have continued to show that maps of threshold tation, and these sites are intermingled with sites where stim-
responses evoked by ICMS include the same features. Two ulation evokes other movements of the same body part, or
examples are shown in Fig. 4. In anesthetized owl monkeys movements of adjacent body parts, or contractions of other
(Fig. 4A), although a general within-limb somatotopic gradient nearby muscles. At the same time, gradual somatotopic gradi-
could be appreciated (distal representation stronger posterolat- ents—indicating gradual shifts in the part(s) most heavily
erally and proximal representation stronger anteromedially), represented— can often be appreciated in ICMS maps of the
movement of a given part (such as the digits) was evoked by forelimb representation. Similar features appear in ICMS maps
ICMS at multiple foci scattered over a considerable portion of of the face representation as well (Huang et al. 1988).
the upper extremity representation, and these foci were inter-
mingled with points at which stimulation elicited movements What is revealed with ICMS?
of other parts of the limb (Gould et al. 1986). In awake
stump-tailed monkeys (Macaca arctoides, Fig. 4B), although At this point, one might come away with the interpretation
the thumb had more representation laterally, movement of any that M1’s somatotopic organization consists of a mosaic of
given digit was evoked by ICMS at foci scattered over a large small discrete zones, with each movement or muscle repre-
portion of the upper extremity representation, and the territory sented in multiple scattered zones. The large and overlapping
from which ICMS evoked movement of a given digit over- cortical territories demonstrated by the older methods of cor-
lapped with the territory from which ICMS evoked movement tical surface stimulation then could have resulted from stimu-

of any other digit (Kwan et al. 1978). A similar pattern of lation of many of these tiny zones at the same time. The extent
scattered threshold foci for individual muscles, intermingled to which the efferent zones mapped by threshold ICMS are
with foci for other muscles, has been described by recording actually discrete, however, is called into question by two major
evoked EMG activity during ICMS in squirrel monkeys (Do- considerations.
noghue et al. 1992; Strick and Preston 1978, 1982), macaques First, even with ICMS, stimulation does not occur entirely at
(Humphrey 1986), and baboons (Waters et al. 1990). Thus a single point. Many of the corticospinal neurons that discharge
even with threshold ICMS, a particular movement of a given in response to ICMS are excited directly at the soma or axon
body part, or a contraction of a specific muscle, is evoked by hillock, and these neurons do indeed lie within a small zone
FIG. 4. Intracortical microstimulation maps. A: a selected portion is shown of the threshold intracortical microstimulation
(ICMS) map of the left hemisphere M1 in an anesthetized owl monkey, a species in which M1 lies on the surface of a relatively
lissencephalic cortex. Black dots mark stimulated points, and solid lines surround groups of points where stimulation evoked
movements of the same body part. Added colors emphasize regions where threshold ICMS evoked movements of different parts
of the upper extremity. Note that movements of a given part of the upper extremity, exemplified by the digits, were evoked from
several scattered foci, intermingled with foci from which movements of other parts were elicited. At the same time, an overall
somatotopic gradient [with heavier representation of the more distal parts (digits, wrist, and forearm) posterolaterally; and heavier
representation of the more proximal parts (shoulder and elbow) anteromedially] can be appreciated. The rectangle on the
hemispheric outline inset at bottom right indicates the region enlarged. ANK, ankle; CH, chin; Dig, digits; EL, elbow; FA, forearm;
M, mouth; NO, nose; SH, shoulder; TR, trunk; VIB, vibrissae; W, wrist (modified from Gould et al. 1986). B: map of locations
from which ICMS evoked movements of different fingers in an awake stump-tailed monkey. Different digits are indicated by 1 ⫽
thumb through 5 ⫽ little finger. Letters indicate the type of movement: f, flexion; e, extension; a, adduction; b, abduction. Flexion
of digits 2 through 5, for example, is denoted “25f.” Note that representation of movements of different digits are largely
intermingled, although the thumb tended to have a heavier representation more laterally (down). The anterior bank of the left central
sulcus has been unfolded, with the depth of the sulcus represented by the solid vertical line at right (length, 10 mm), and the lip
of the anterior bank represented by the dotted vertical line. Dashed vertical lines represent the borders between Brodmann’s areas,
and the outer dashed curve encloses the entire upper extremity representation (redrawn from Kwan et al. 1978).

close to the electrode tip. As noted above, in cat M1, low- being mapped with threshold electrical stimulation? Threshold
amplitude ICMS pulses have been estimated to directly excite ICMS mapping in M1 entails placing the electrode tip at a
on the order of 28 pyramidal neuron somata within a radius of certain point in or near layer V, and gradually adjusting stim-
88 ␮m (Stoney et al. 1968). In the baboon, a 0.2-ms ⫻ 5-␮A ulus strength until on half of stimulation trials the discharge of
pulse delivered in layer V was estimated to directly excite some motor units is just detected, either by recording EMG
90 –900 small and 1–5 large pyramidal neurons within a radius activity, or by having enough motor units discharge to produce
of 40 –125 ␮m, whereas at 90 ␮A, a generous estimate of the an externally observable movement. With either assay, the
effective spread of stimulating current was only 0.6 mm experimental observation means that the evoked output from
(Andersen et al. 1975). Direct excitation of neuronal somata or M1 to a particular muscle (or potentially a combination of
axon hillocks by ICMS thus is reasonably focal. muscles when observing movement) was greater than the out-
Shortly after ICMS came into use, however, investigators put to other muscles, not that output occurred to that muscle
realized that the same pulses could excite additional cortico- alone. Output may well have occurred to motoneurons of other
spinal neurons at greater distances through two mechanisms. muscles; such output to other muscles simply was insufficient
One mechanism is direct excitation of the intracortical collat- to cause them to discharge (or to discharge enough to produce
erals of pyramidal tract axons, which may extend horizontally observable movement). The apparently discrete zones of ICMS
up to 1 mm away from the soma (Asanuma et al. 1976).1 A maps obtained with threshold stimuli thus represent the quan-
second mechanism is indirect, trans-synaptic excitation. In- titatively greatest outputs, not qualitatively exclusive outputs.
deed, the greatest part of the descending volley produced by

What happens, then, if the stimulus strength is increased
ICMS results from such trans-synaptic excitation of cortico- beyond threshold? Are outputs to additional muscles revealed?
spinal neurons, even when the stimulating electrode is within Phillips and colleagues recorded simultaneously from single
layer V and currents are as low as 5 ␮A or less (Jankowska et motor units in the thenar eminence (thumb muscles), in the first
al. 1975b). Moreover, repetitive ICMS of the same intracortical dorsal interosseous muscle (FDI, an index finger muscle), and
point at frequencies of 200 – 400 Hz, the type of stimulation in extensor digitorum communis (EDC, which extends the 4
needed to evoke detectable movement or EMG activity in the fingers)2 while using ICMS to map the forelimb region of
studies described above, produces powerful temporal summa- baboon M1 (Andersen et al. 1975). Threshold stimulation at
tion of this trans-synaptic excitation (Asanuma et al. 1976; most points evoked discharge in only one of the three motor
Jankowska et al. 1975b). Although most trans-synaptically units. Using currents up to 80 ␮A, however, they found that the
excited corticospinal neurons probably lie relatively close to three motor units recorded from these three muscles each could
the ICMS microelectrode, some somata may be more distant. be brought to discharge with ICMS at many points spread over
Horizontally extending axon collaterals can produce excitatory a wide cortical territory, and that the total territories from
postsynaptic potentials (EPSPs) in M1 pyramidal tract neurons which each motor unit could be discharged overlapped exten-
within a 1- to 2-mm radius (Asanuma and Rosen 1973; Mat- sively (Fig. 5). Their calculations showed that spread of the
sumura et al. 1996), and intracortical microstimulation can higher currents did not account for the overlap. Even at 90 ␮A,
excite some pyramidal tract neurons within this radius (Baker a current larger than they routinely employed, a generous
et al. 1998). While most of the effects of ICMS result from estimate of the spread of current effective for direct stimulation
excitation of pyramidal tract neurons quite close to the micro- of somata and axons was only 0.6 mm, while the motor unit
electrode, a penumbra of other pyramidal tract neurons may be territories overlapped several millimeters. Hence the colony
excited as well. Quantitative estimates of what fraction of of Betz cells whose output excited each motor unit necessarily
observed muscle contraction or movement results from direct was spread over a considerable cortical territory, largely inter-
excitation of local somata versus excitation of penumbral neu- mingled with the colonies of Betz cells exciting the motor
rons are not available. units of the other muscles.3 Similar findings were obtained
A modified ICMS technique recently has been developed with intracellular recordings from hindlimb motoneurons
that avoids the temporal summation of repetitive stimulation at (Jankowska et al. 1975a).
high frequency (⬃300 Hz) used in conventional ICMS to Subsequently, several investigators have confirmed that
produce detectable output effects in quiescent animals. In ICMS maps show multiple scattered loci from which threshold
stimulus-triggered averaging (StTA), single ICMS pulses are stimulation evokes movement about a particular joint, or EMG
delivered at much lower frequencies (10 –20 Hz) while awake activity in a particular muscle. In between are scattered thresh-
monkeys perform active movements, and triggered averaging old loci for other movements or muscles, forming a “complex
then is used to extract the effects of these pulses from ongoing mosaic.” As stimulus intensity is increased systematically
voluntary EMG activity (Cheney and Fetz 1985). Because the above threshold, however, movements are produced at addi-
temporal summation of EPSPs is eliminated, StTA probably tional joints (Sessle and Wiesendanger 1982), or contractions
produces much less of its effect via indirect, trans-synaptic
excitation. Yet maps made with StTA continue to show large 2
The large spatial extent of the “colony” of layer V neurons projecting to
cortical territories for individual muscles that overlap exten- the EDC motoneuron pool of macaques recently has been demonstrated
sively with the cortical territories of other muscles (Park et al. anatomically by retrograde transneuronal transport of rabies virus injected into
2001). the EDC muscle belly (Rathelot and Strick 2000).
3
This brings us to the second consideration: exactly what is These authors did not consider excitation of additional, penumbral neurons
via horizontal axon collaterals or indirect trans-synaptic excitation. Even if one
considers a 2-mm penumbra of lesser excitation, however, the overlap they
1
Indeed, recent studies of electrical excitation in slices of rat visual cortex demonstrated for cortical territories of different muscles is too extensive to
indicate extracellular stimulation excites axonal branches more readily than attribute entirely to spread of excitation and therefore indicates intermingling
axon initial segments or somata (Nowak and Bullier 1998a,b). of corticospinal neurons exciting different muscles.

2132 M. H. SCHIEBER

FIG. 5. Convergence and overlap demonstrated with ICMS. Results of ICMS at currents up to 80 ␮A in 12 electrode
penetrations (denoted A through N) down the anterior wall of a baboon’s central sulcus while recording 3 single motor units: one
in extensor digitorum communis (EDC, which extends all 4 fingers, radial nerve innervation); another in the thenar muscles
(Thenar, which act only on the thumb, median nerve innervation); and a 3rd in the 1st dorsal interosseous (FDI, which acts on the
index finger, ulnar nerve innervation). In each penetration, black dots indicate locations where ICMS was ineffective, whereas
numbers indicate threshold current (␮A) for evoking discharge of the motor unit. Lateral is to the viewer’s left; medial to the right.
With currents up to 20 ␮A (red), multiple small zones from which each motor unit could be discharged were identified. Although
the zones for the different motor units were largely interdigitated, on close inspection these small zones also overlapped to some
degree. At higher currents up to 40 (orange) and then 80 ␮A (yellow), the small zones for each motor unit expanded and coalesced
into large cortical territories, increasing their mutual overlap. Current spread could not account for this degree of convergence and
overlap in the cortical territories of these 3 motor units, which each were served by different peripheral nerves and each acted on
different digits (modified from Andersen et al. 1975).
are evoked in more and more muscles (Donoghue et al. 1992), fine, relatively independent movements (Phillips and Landau
so that the loci for any particular muscle tend to expand and 1990). Shortly after Phillips and colleagues had articulated the
coalesce, revealing the large total territory representing that concept of convergence from wide M1 territories onto spinal
muscle, which overlaps extensively with the territories repre- motoneurons, evidence appeared demonstrating that the output
senting other muscles (Humphrey 1986; Sato and Tanji 1989). projections from single M1 neurons often diverge to innervate
This expansion and coalescence into large and overlapping the motoneuron pools of more than one muscle.
territories cannot be attributed entirely to current spread and Anatomic evidence of such divergence was obtained by
indirect, trans-synaptic excitation. Thus ICMS, like surface filling single corticospinal axons with horseradish peroxidase
stimulation, indicates convergence of M1 outputs from large (HRP), revealing that collateral branches of a single cortico-
and overlapping M1 territories onto different muscles or move- spinal axon often ramified over several spinal segments pro-
ments. viding terminal arbors in the motoneuron pools of up to four
Because even ICMS involves some spread of current to
muscles (Fig. 6A) (Shinoda et al. 1981). Physiologic evidence
multiple neurons, and because such current can excite neurons
of divergence came from the use of spike-triggered averaging
both directly and indirectly, the question of whether stimula-
tion at a single “point” in M1 actually produces output to more of rectified EMG activity to identify functional, short-latency
than one muscle cannot be resolved with extracellular electrical connections from M1 neurons to spinal motoneuron pools (Fig.
stimulation. The ideal experiment for resolving this question 6B) (Fetz and Cheney 1978, 1980). Many single M1 neurons
(recording intracellularly from the spinal motoneurons of sev- produced postspike effects, indicative of relatively direct cor-
eral muscles while stimulating intracellularly in the somata of ticomotoneuronal connections, in up to six different forearm
single corticospinal neurons in M1) remains technically inac- muscles. Spike-triggered averaging also has shown divergent
cessible even now. In the 1980s, however, separate lines of outputs from M1 neurons controlling the intrinsic muscles of
evidence developed rendering much of the previous arguments the hand; those used in the finest of relatively independent
moot. movements (Buys et al. 1986; Lemon et al. 1986). Further-
more, a recent study indicates that the functional connections
DIVERGENCE
of single M1 neurons may diverge, not only to different mus-
cles moving the fingers and wrist, but also to muscles moving
For many years neuroscientists generally believed that a the elbow and shoulder (McKiernan et al. 1998). These diver-
given corticospinal neuron made monosynaptic connections to gent projections from single M1 neurons obviously constrain
the motoneurons of only one muscle. These specific connec- the degree to which M1’s output can be organized in a strict
tions to particular muscles enabled the “upper motor neurons” within-limb somatotopy. The set of muscles receiving the
in M1 to selectively activate the muscles needed to perform output of a single M1 neuron may act on multiple fingers; on

the fingers and the wrist; or even on the fingers, wrist, elbow, independently. By providing site-specific outputs to selected
and shoulder. elements, the somatotopic map in M1 was thought to act like a
piano keyboard on which higher levels of the cortex could play
HORIZONTAL INTERCONNECTIONS out motor programs. This notion has been supported by ana-
tomic studies demonstrating that the majority of intracortical
The concept of a strict somatotopic organization implied that connections within M1 are relatively local, spreading horizon-
different sites within M1 acted on their output targets relatively tally over a radius of only 1–2 mm. Lesions made by passing
a microelectrode through monkey M1 cortex radially (normal
to the pial surface) resulted in dense fiber degeneration spread-
ing horizontally from the lesion over a radius of 200 –300 ␮m,
and less densely over a radius of 2–3 mm (Gatter and Powell
1978). Intracellular injections of HRP into cat pyramidal tract
cells showed axon collaterals spreading horizontally in layers
V and VI, densely over a radius of 0.5– 0.8 mm, and less
densely over 1.5–2.0 mm radius, with a few extending as far as
2–3 mm from the soma (Landry et al. 1980). Neurobiotin-filled
cat pyramidal neurons in layers II and III extend horizontal
axons collaterals within these layers for up to 1 mm (Keller and

Asanuma 1993).
These anatomic findings are consistent with studies demon-
strating that the strongest physiologic interactions are found
between M1 neurons separated by 1–2 mm. Low-amplitude (4
␮A) ICMS in cat M1 evokes monosynaptic postsynaptic po-
tentials (PSPs) in neurons within only a 0.5-mm horizontal
radius, and polysynaptic PSPs chiefly within 1-mm radius
(Asanuma and Rosen 1973). Spike-triggered averaging of in-
tracellular potentials in monkey M1 likewise has shown that
EPSPs and inhibitory postsynaptic potentials (IPSPs) are stron-
gest and most common within 1–2 mm (direct rather than
horizontal distance) of the triggering neuron (Matsumura et al.
1996). The observations that two sequential 20-␮A ICMS
pulses delivered through the same electrode produce intracor-
tical facilitation of evoked EMG, whereas sequential pulses
delivered through electrodes separated horizontally by 1.5–2.0
mm do not also support the notion that the strongest physio-
logic interactions between M1 neurons occur within 1.0 mm,
although the same ICMS pulses do affect the discharge of some
pyramidal tract neurons 1.5–2.0 mm away (Baker et al. 1998).
Similarly, synchronous discharges in the action potential trains
of two neurons (indicating shared or serial inputs) are found
more commonly when the two neurons are close enough to be
recorded from the same microelectrode, and the likelihood of
finding synchronous discharge decreases with horizontal sep-
aration until synchrony is rarely detected between neurons
FIG. 6. Divergence in the projection of single corticospinal neurons. A: a

horseradish peroxidase (HRP)–filled corticospinal axon has been reconstructed
in the transverse plane of the ventral horn of the monkey spinal cord. The cord
midline and central canal are to the left; the lateral column to the right. The
filled corticospinal axon enters the spinal gray matter from the lateral column
and branches repeatedly, ultimately giving off terminal ramifications in the
outlined motoneuron pools of 4 different muscles (reproduced from Shinoda et
al. 1981). B: averages of rectified electromyographic (EMG) activity are shown
from 6 muscles [extensor digitorum secundi et tertii (ED23), extensor carpi
ulnaris (ECU), extensor digitorum quarti et quinti (ED45), extensor digitorum
communis (EDC), extensor carpi radialis longus (ECRL), and extensor carpi
radialis brevis (ECRB)] that act on the wrist and/or fingers in macaque
monkeys. Each average of rectified EMG was triggered from several thousand
spikes discharged by the simultaneously recorded M1 neuron whose averaged
action potential is shown in the top trace. The brief (⬃10 ms) peaks that appear
in each of the 1st 4 EMG traces shortly after the neuron spike indicate that
motoneurons innervating these 4 muscles received synaptic excitation at a
short and fixed latency following the discharge of action potentials by the M1
neuron (modified from Fetz and Cheney 1980).

2134 M. H. SCHIEBER
separated by more than 2.0 mm (Grammont and Riehle 1999; injections, including some double-labeled neurons (Tokuno
Kwan et al. 1987; Riehle et al. 1997; Smith and Fetz 1989). and Tanji 1993).
Horizontal interconnections extending 1–2 mm may mediate Horizontally projecting axon collaterals interconnecting the
interactions between M1 neurons contributing to the control of entire upper extremity representation have been demonstrated
different muscles acting about the same joint (Capaday et al. as well in the cat and the rat, where the collaterals have been
1998), or neighboring joints of the same extremity (Kwan et al. shown to arise predominantly from pyramidal neurons in layers
1987). III and V, and to have predominantly excitatory, glutamatergic
Although the strongest intracortical interconnections thus effects (Aroniadou and Keller 1993; Keller 1993; Weiss and
occur within a 1-mm radius of a given pyramidal neuron, Keller 1994). In monkey M1, inhibitory, GABAergic neurons
recent anatomical studies have shown that many M1 neurons have predominantly vertically oriented projections (DeFelipe
extend axon collaterals even further horizontally, interconnect- and Jones 1985), although the axons of GABAergic basket
ing much larger regions of M1 (Fig. 7). HRP injections in the cells may project horizontally for 1–3 mm. Furthermore, the
ICMS-defined digit region of monkey M1 revealed that neu- effective range of intracortical inhibition may be much greater
rons near the injection site extended terminal arbors throughout (Kujirai et al. 1993), in part because local inhibitory interneu-
the upper extremity region, including the territory where rons may receive excitatory inputs from long-range horizontal
threshold ICMS had evoked movements of the shoulder, el- projections within M1 (Jacobs and Donoghue 1991). Long-
bow, or wrist (Huntley and Jones 1991). Conversely, neuronal range horizontal interconnections within M1 thus provide a
somata throughout the upper extremity representation were substrate for information to be interchanged through a network

filled retrogradely by the HRP injection in the digit region, distributed widely through the M1 upper extremity represen-
indicating that neurons throughout the upper extremity territory tation, again limiting the degree to which a particular M1 site
send axon collaterals into a single focus within the digit rep- can be associated with control of a particular body part.
resentation. When the injection was placed laterally, close to Besides long-range intrinsic connections within M1, afferent
the face representation, labeled terminals and somata still were inputs to M1 also show considerable horizontal distribution.
found in the ICMS-defined shoulder representation, 7– 8 mm Given that any particular locus within M1 tends to receive
medial to the injection site. Similarly, when Fast Blue (FB) was somatosensory input from the same body part moved by ICMS
injected in the digit representation, and Diamidino Yellow at the locus (Murphy et al. 1978; Rosen and Asanuma 1972),
(DY) was injected 7– 8 mm away in the shoulder region of it is not surprising that somatosensory inputs to M1 also have
monkey M1, retrogradely labeled FB and DY somata were a scattered and intermingled distribution (Lemon 1981; Wong
found intermingled throughout the M1 cortex between the two et al. 1978). In large part, somatosensory inputs to M1 arrive
FIG. 7. Horizontal interconnections in the M1 upper extremity representation. After using ICMS to map the M1 upper extremity
representation in a macaque monkey’s left hemisphere, HRP was injected in the low-threshold digit representation at the site
indicated by the large, filled black circle with surrounding coarse-stippled penumbra. This injection resulted in widespread terminal
labeling (fine stippling in A) and retrograde filling of neuronal somata (small black dots in B). ICMS was delivered at sites indicated
by the large black dots in both A and B. Regions where stimulation at many contiguous sites elicited movement of the same body
part are delimited with dashed lines, exceptional sites being indicated individually. Stars indicate points where stimulation up to
40 ␮A failed to evoke observable movement. The solid line at the right indicates the central sulcus, and data from its anterior bank
have been represented as if projected to the hemisphere’s surface. Scale bars at bottom represent 1 mm. Anterior is to the left;
posterior, right; medial, up; lateral, down (modified from Huntley and Jones 1991).

via short U-fibers from the primary somatosensory cortex, theless, horizontal connections intrinsic to the M1 upper ex-
fibers that arborize over a considerable rostrocaudal distance in tremity representation may contribute to synchronous LFP
M1. In macaques, these corticocortical axons may give off two oscillations, associating the widespread neurons needed to per-
to three terminal arborizations separated by up to 800 ␮m form a coordinated movement of the entire extremity.
(DeFelipe et al. 1986). Similar arborization patterns have been
found for corticocortical afferents to M1 from area 5 in the cat DISTRIBUTED ACTIVATION
(Kakei et al. 1996). Thalamocortical afferents to M1 from the
cat ventroanterior and ventrolateral (VA/VL) nuclear complex For many years, authorities debated whether it was muscles
distribute their terminal fields even more extensively, some per se, or the movements they produced, that were represented
covering areas up to 5.0 ⫻ 4.8 mm (almost 25 mm2) in somatotopically in M1 (Phillips 1975). The convergence of M1
rostrocaudal and mediolateral dimensions (Shinoda et al. outputs to single motoneuron pools from wide and overlapping
1993). Both corticocortical and thalamocortical afferents thus cortical territories, and the divergence of output from single
distribute their information widely in the M1 forelimb repre- M1 neurons to multiple motoneuron pools, both necessarily
sentation. constrain any somatotopic representation of individual muscles
The functional role played by long horizontal connections in M1. The overlapping cortical territories of different muscles
within M1 remains uncertain. Nevertheless, physiologic stud- raise the possibility, however, that different combinations of
ies in awake behaving animals have demonstrated a number of activity in multiple muscles are represented at different cortical
types of correlations between the discharge of M1 neurons that sites. Voluntary movements, even movements of a single joint

may in part be mediated by these long horizontal interconnec- or a single finger, typically involve simultaneous contractions
tions. One form of correlation between relatively distant M1 of multiple muscles (Beevor 1903; Schieber 1995). The simul-
neurons has been demonstrated by averaging the intracellular taneous contractions of a such a set of muscles producing
(IC) potential of one neuron triggered from the extracellular movement of one body part might be represented at one loca-
(EC) action potentials of a second neuron (Matsumura et al. tion in M1, while the simultaneous contractions of a partially
1996). These averages frequently reveal a broad depolarization overlapping set of muscles producing movement of a different
of the IC neuron straddling the triggering spikes of the EC body part might be represented at a different location. Al-
neuron. Such average synchronous excitation potentials though electrical stimulation mapping had also suggested over-
(ASEPs) indicate that the IC and EC neurons both receive lap of movement representations (above), electrical stimulation
some sort of synchronous excitation. ASEPs, although most is unlikely to mimic accurately the natural cortical activation
common and most intense in pairs of neurons separated by ⬍2 that occurs during voluntary movements.
mm, also have been found in pairs of neurons separated by up Since the 1960s, a number of techniques (including single
to 4.5 mm in monkey M1. neuron recording, functional neuroimaging, and magnetoen-
A second type of long-range correlation has been demon- cephalography) have become available for probing cortical
strated by examining the trial-by-trial variation in the discharge activity during voluntary movements performed by awake sub-
of monkey M1 neurons averaged over 600 ms during a reach- jects. A well-ordered, discrete somatotopic organization of M1
ing task (Maynard et al. 1999). The trial-by-trial variation in would imply that movements of different body parts involve
average discharge rate of two neurons was more likely to be activation of spatially distinct regions of M1, with these re-
correlated if the two neurons had similar preferred directions, gions arrayed in somatotopic order. Somatotopically ordered
suggesting that functionally similar neurons receive shared activation during voluntary movements should be demonstra-
inputs that fluctuated from trial to trial. The strength of such ble with these modern techniques.
correlations did not depend on the horizontal distance between Experimental studies examining M1 activity during move-
the two neurons, however. Although interneuronal separations ments of different parts of the upper extremity, however, have
of only up to 2 mm were examined, that the correlation revealed relatively little evidence of activation in spatially
strength was independent of separation distance suggests that distinct regions of M1. In monkeys performing individuated
this type of correlation extends beyond 2 mm. movements of each finger and of the wrist, single neurons were
The most extensive evidence of long-range interactions found to discharge in relation to movements of several differ-
within M1, however, comes from studies of local field potential ent fingers, which obviously constrains the degree to which
(LFP) oscillations, which occur synchronously over regions of movements of different fingers could be represented in spa-
the M1 upper extremity representation extending 14 mm me- tially distinct regions of M1 (Schieber and Hibbard 1993).
diolaterally along the central sulcus of monkeys (Donoghue et Moreover, the M1 territories containing neurons active during
al. 1998; Murthy and Fetz 1992, 1996a). These LFP oscilla- movements of different fingers were virtually coextensive,
tions are coherent with simultaneous oscillations in EMG ac- with little evidence of a somatotopic shift in the center of
tivity (Baker et al. 1997; Hari and Salenius 1999). Neurons at activity from lateral to medial for movements of the thumb
sites separated by up to 10 mm have been found to have through little finger and wrist (Fig. 8). Similarly, functional
oscillatory modulation of their discharge in phase with these magnetic resonance imaging (fMRI) in humans has shown
LFP oscillations, and pairs of such neurons often show peaks in extensive overlap of the cortical territories activated during
cross-correlograms of their spike discharges recorded during performance of thumb, index finger, ring finger or wrist move-
LFP oscillations (Baker et al. 1999; Murthy and Fetz 1996b). ments (Sanes et al. 1995). Magnetoencephalography in humans
The fact that such correlations during LFP oscillations can be likewise has shown that the dipole sources of the neuromag-
found between neurons in the left and right M1 indicates that netic fields generated during movements of different digits are
intrinsic horizontal connections are unlikely to be the sole not arrayed in somatotopic order, either in a single subject or
anatomic basis for such widespread synchronization. Never- averaged across multiple subjects (Cheyne et al. 1991; Salenius

2136 M. H. SCHIEBER
that the territory active during movements of multiple fingers

should be larger than the territory activated during movement
of a single digit. When this hypothesis has been tested exper-
imentally, however, the extent and amplitude of activation in
the primary sensorimotor cortex has been found to be signifi-
cantly larger during movement of a single finger than during
simultaneous movement of multiple fingers (Kitamura et al.
1993; Remy et al. 1994). Such results indicate that the process
of moving multiple fingers is not simply the sum of activating
multiple separate M1 territories, each controlling a different
finger; rather, moving a single finger without the others re-
quires more M1 activity than moving multiple fingers simul-
taneously. Presumably, such extra activation occurs because,
besides controlling the motion of the one finger, M1 actively
participates in stabilizing other parts of the upper extremity
during the individuated movement of a particular finger (Hum-
phrey and Reed 1983; Schieber 1990).
Could the distributed activation observed in awake behaving

subjects reflect activation of somatotopically organized cortex,
with one region producing the movement and other regions
stabilizing other body parts? If one considers only studies of
activation in awake behaving subjects, this interpretation cer-
tainly is possible. But ICMS should have demonstrated such an
underlying somatotopic organization (see Figs. 4 and 5), and
the divergence of output from single M1 neurons to muscles
that move all four fingers and the wrist (Fig. 6), or to muscles
acting on both the digits and the shoulder (McKiernan et al.
1998), would certainly limit the degree of somatotopic segre-
gation of these representations. Distributed representation pro-
vides a more parsimonious interpretation of all these observa-
tions considered together.
Several studies have demonstrated comparatively small, so-
matotopically ordered shifts in the location of activation during
FIG. 8. Distributed activation in M1 during finger movements. A: colored
movements of different parts of the upper extremity. It must be
spheres each represent a single neuron recorded in the left hemisphere M1 as recognized, however, that these shifts are detected by using
a monkey performed individuated movements (flexion or extension) of each analytic approaches that minimize the contribution of activa-
right-hand digit and of the right wrist. Each neuron was consistently related to tion common to different movements. For example, somato-
at least 1 movement, although most neurons were related to multiple different topically ordered shifts may be detected in the centroids of
finger and/or wrist movements. The sphere representing each neuron is cen-
tered at the location of the recorded neuron in the anterior bank of the central activation calculated for movements of different fingers. These
sulcus, with the hemispheric surface above, white matter below, lateral to the shifts are small, however, compared with the total spatial
viewer’s right and medial to the left. Each sphere is sized according to its extent of the territory activated. In monkeys, the centroids of
greatest change in discharge frequency during any of the movements; the white activation during different finger and wrist movements were
spheres at left constitute a scale from 0 to 200 spikes/s, with centers 1 mm
apart. Each sphere representing a neuron is colored according to the movement
found to be spread over 2 mm along the central sulcus, whereas
for which that neuron’s greatest discharge occurred: thumb, red; index finger, the field containing active neurons extended 8 –9 mm (Fig. 8)
orange; middle, yellow; ring, green; little, blue; wrist, violet. Neurons best- (Schieber and Hibbard 1993). In humans, centroids of fMRI
related to movements of each digit or the wrist were intermingled throughout activation for movements of different fingers may be spread
the same cortical territory. B: centroids of discharge frequency changes cal- over 2.46 mm (no greater than the thickness of the cortex
culated for each flexion movement and each extension movement are shown in
the same coordinate system as in A, with the scale of white spheres as a visual itself!) (Beistener et al. 2001; Hlustik et al. 2001; Indovina and
anchor. Rather than shifting progressively across the field of active cortex for Sanes 2001), whereas the total extent of the hand representa-
thumb through little finger and wrist movements, these centroids all are tion along the central sulcus is roughly 50 mm (Hlustik et al.
clustered together in the center of the field, with only a slight shift for 2001; Penfield and Boldrey 1937). In both species, comparing
movements of different digits or the wrist, reflecting the extensive overlap of
the representations of different movements (modified from Schieber and
the spatial separation of the centroids with the spatial extent of
Hibbard 1993). the hand representation indicates that the territories activated
during movements of different fingers must overlap exten-
et al. 1997). These studies all indicate that movements of sively.
different fingers are not mediated by activity in different, Analytic techniques that make even less use of the activation
spatially segregated regions, somatotopically arrayed in M1. common to different movements have demonstrated greater
Rather, they suggest that movement of any finger is mediated apparent separation. Although the territory of fMRI activation
by the activity of neurons widely distributed in the M1 upper during thumb movement overlaps extensively with that during
extremity representation. little finger movement, difference images that subtract away
Strict somatotopic organization of M1 also would predict the shared activation have shown that the activation peak

during thumb movements is lateral to that during little finger cus (Schieber and Poliakov 1998). Similarly, when muscimol
movements (Kleinschmidt et al. 1997). Similarly, when the was injected at loci where ICMS evoked thumb and index
activation peaks during thumb, index finger, wrist, elbow, and finger movements, movements of the whole hand were im-
shoulder movements were compared using positron emission paired (Brochier et al. 1999). Microinfarction of ICMS defined
tomography (PET), a somatotopic progression from lateral to hand representation in squirrel monkeys resulted not only in
medial was demonstrated (Grafton et al. 1993). These obser- decreased use of the hand, but also in tonic flexion at the elbow
vations become consistent with observations of distributed and adduction of the extremity close to the torso, similar to the
activation, as well as with observations of convergence, diver- involuntary tonic posturing of the upper extremity seen in
gence, and horizontal interconnections, when the gradual shift human patients after much more extensive lesions of M1 (Friel
in peak activation or centroid of activation is recognized to be and Nudo 1998). The deficits produced by controlled lesions in
present on a base of extensively overlapping representation. animal studies, like those resulting from lesions produced by
disease in humans, suggest that control of each finger, and of
PARTIAL INACTIVATION
each more proximal joint, is widely distributed in the M1 upper
extremity representation.
A strictly somatotopic organization of M1 also would pre-
dict that in some instances lesions should affect certain parts of PLASTICITY
the upper extremity without affecting others. In human pa-
tients, where lesions of M1 may be produced by a variety of Observations indicative of what we now call plasticity are

disease processes, the resulting upper extremity weakness af- almost as old as stimulation mapping of M1. In their classic
fects distal strength in the fingers and wrist more profoundly study of somatotopic organization of M1 in the great apes, for
than proximal strength in the shoulder and elbow (Bucy 1949; example, Leyton and Sherrington (1917) took pains to describe
Colebatch and Gandevia 1989). Uncommonly, more selective the “functional instability of cortical motor points.” They
lesions weaken the fingers and wrist much more profoundly found that after the movement evoked by stimulation of a given
than the elbow and shoulder (Foerster 1936). Even in these point was first identified, intervening stimulation of the same
cases, however, some weakness is evident at these proximal point or other nearby points could result in facilitation, rever-
joints, unless the weakness of the hand itself is minimal. Even sal, or deviation of the movement evoked when stimulation of
more uncommonly, human patients have been reported with the given point subsequently was repeated. These investigators
weakness greater in some fingers than in others. Most often, the inferred that “. . . the functional instability of cortical motor
thumb is the weakest digit, with some weakness of the index as points are indicative of the enormous wealth of mutual asso-
well (Lee et al. 1998; Terao et al. 1993). Greatest weakness of ciations existing between the separable motor cortical points,
the thumb (and index) could result from a greater representa- and those associations must be a characteristic part of the
tion of the thumb and index throughout the M1 hand area, machinery by which the synthetic powers of that cortex are
rather than selective involvement of a region controlling only made possible.” When M1 was considered to contain a point-
the thumb. Other cases have been reported, however, in which to-point somatotopic map of body parts, movements, or mus-
the little and ring fingers were weakest (Foerster 1936; Kim cles, with each corticospinal neuron monosynaptically con-
2001; Phan et al. 2000; Schieber 1999). Notably absent are nected to one and only one spinal motoneuron pool, the
cases in which the index, middle, or ring fingers were the possibility of plastic reorganization in M1 seemed remote. The
weakest. Human cases thus suggest that, rather than discrete convergence, divergence, horizontal interconnections, and dis-
regions of M1 controlling different parts of the upper extrem- tributed activation described above, however, provide a sub-
ity, control of each part is mediated by an extensive territory strate that would appear capable of considerable plastic reor-
that overlaps with the territories controlling other parts. Nev- ganization.
ertheless, on top of this widely distributed control of each As reviewed in detail elsewhere (Nudo et al. 2001; Sanes
finger, two somatotopic gradients may be present, consistent and Donoghue 2000), in the past decade M1 has been shown to
with the general order suggested by the homunculus. First, the undergo plastic reorganization in response to a variety of
proximal upper extremity is represented more heavily medially changes, including peripheral lesions, central lesions, and mo-
than laterally, while the reverse is true for the distal upper tor skill acquisition. Here we focus only on the latter, which
extremity. Second, within the distal representation, the thumb may be most relevant to the normal organization of somato-
and index are represented more heavily laterally than medially, topic representation in M1. In a variety of motor skill acqui-
while the little and ring fingers are represented more heavily sition paradigms, the M1 representation of the trained body
medially than laterally. parts has been shown to enlarge, typically at the expense of the
The exact location and extent of lesions in human cases, of representations of less trained body parts. In rats trained to
course, cannot be controlled experimentally. Relatively few reach and grab small food pellets, for example, the ICMS
investigations in experimental animals have attempted to cor- defined M1 representation of digit and wrist movements was
relate the location of a lesions within the M1 upper extremity expanded at the expense of elbow and shoulder movement
representation with the resulting motor deficits in the upper representation (Kleim et al. 1998). In monkeys trained to
extremity. In monkeys performing individuated finger move- retrieve small objects, ICMS mapping likewise revealed ex-
ments, however, partial inactivation of the M1 hand area pro- pansion of the digit representation, whereas in monkeys trained
duced by intracortical injection of the GABAA agonist, mus- to perform forearm pronation/supination movements the rep-
cimol, impaired some finger movements more than others, but resentation of forearm movements expanded (Nudo et al.
which finger movements were impaired was unrelated to the 1996). These changes are progressive as training continues,
mediolateral location of the inactivation along the central sul- and reverse after training stops (Fig. 9).

2138 M. H. SCHIEBER

FIG. 9. M1 Reorganization in relation to motor training. A: after initial ICMS mapping of the distal forelimb representation
(Baseline), a squirrel monkey was trained for 11 days on a Kluver board and then re-mapped (Training I), with little change in the
total area devoted to digit (red), wrist/forearm (green), digit and wrist/forearm (yellow, DIG ⫹ W/FA), digit and more proximal
(blue, DIG ⫹ PROX), or wrist/forearm and more proximal (purple, W/FA ⫹ PROX) movements. After additional training on the
Kluver board for 39 days, re-mapping showed increases in the percent of the total distal forelimb area devoted to movements used
in retrieving food morsels from the small wells on the board: digit and wrist/forearm, finger flexion and wrist extension, and finger
flexion/extension movements (Training II). Then, after 4 mo without practice, re-mapping showed a reversion of these changes back
to baseline (Extinction), and finally after another 30 days training, re-mapping showed that similar changes had occurred again
(Reaquisition). Only points from which stimulation evoked movements of the digits, wrist, or pronation/supination movements of
the forearm are shown in these maps; points eliciting only movements of the elbow and/or shoulder are not included, although they
typically surrounded the distal forelimb representations anteriorly (up), laterally (left) and medially (right) as indicated by “prox”
in the baseline map. B: bargraphs show the percentage of the total distal forelimb representation in each map from which specific
movements were elicited in each phase of the study (modified from Nudo et al. 1996).
Additional evidence obtained in human subjects indicates learning and practicing a particular skill, then reorganization is
that M1 reorganization occurs both within a single session and likely to be proceeding continuously as each individual per-
over the longer term needed to acquire a complex skill. When forms the motor tasks used frequently in their daily life. The
normal human subjects, initially unaware of any sequence, patterns of representation in M1 thus are likely to change as an
practice a repeating sequence of finger movements instructed individual performs more of one motor activity and less of
by visual cues, the amplitude and extent of finger muscle another from day to day. Such a continual process of reorga-
representation assessed by trans-cranial magnetic stimulation nization places yet another constraint on somatotopic organi-
increases in M1 contralateral to the performing hand as the zation in M1.
speed of performance increases over a single day of training
(Pascual-Leone et al. 1994). Several days of such training WHY SHOULD THE PRIMARY MOTOR CORTEX
produce progressive expansion of finger muscle representation, HAVE SO DISTRIBUTED AN ORGANIZATION?
whether the training involves physical practice or only mental
rehearsal (Pascual-Leone et al. 1995). Practicing a finger The ease with which we can comprehend a well-ordered,
movement sequence over several weeks results in greater fMRI discrete, somatotopic representation makes the concept of so-
activation of the M1 hand representation during performance matotopy an attractive organizing principle with which to
of the practiced sequence than during performance of a com- understand the function of the primary motor cortex. Somato-
parable, but unpracticed sequence (Karni et al. 1995). An topy seems so straightforward that it ought be so. The primary
example of very long-term changes related to motor skill is somatosensory cortex (S1) has a well-ordered somatotopic
found in experienced Braille readers, whose M1 representation representation, and the primary visual cortex (V1) has a well-
of the first dorsal interosseous muscle (used to sweep the tip of ordered retinotopic representation. The evidence reviewed
the index finger over Braille letters) is expanded in M1 con- above indicating that within-limb somatotopy in M1 is limited,
tralateral to their reading finger (Pascual-Leone et al. 1993). and that a more complex, widely distributed organization exists
If reorganization of M1 in normal subjects can be driven by instead, therefore is likely to reflect important features of

FIG. 10. Cortical pianos. A: the standard

piano keyboard constitutes a well-ordered
map of musical notes. Here the 42 white
keys have been colored to distinguish each of
them. Although the strict order and single
representation make it easy to locate each
note, these same features make it impossible
for a pianist to play certain combinations of
notes, such as the 5 notes marked by black
dots beneath. B: a nonstandard keyboard can
be created by re-representing each note at
multiple locations and in a wide variety of
orders. While this arrangement appears more
complex, with each note represented over a
wide territory that overlaps with the territo-
ries representing many other notes, this dis-
tributed organization provides ready access
to many more combinations of notes than the

standard keyboard. The 5 adjacent notes
marked by black dots in B, for example, are
the same notes indicated in A.
functional organization in M1.4 I close with speculations as to A second feature of functional organization may have to do
what these features might be. with what needs to be processed simultaneously by M1. The
One such feature may be the dimensionality of the informa- well-ordered representations in S1 (area 3b in particular) and
tion processed in M1. Well-ordered representations exist where V1 are thought to be computationally advantageous because
a two-dimensional receptor sheet (the skin surface or retina, two adjacent receptors are much more likely to receive similar
respectively) can be mapped isomorphically onto the two- input simultaneously than two distant receptors. If a mechano-
dimensional cortex. Movements and the muscles that generate receptor on the thumb is responding to an indenting stimulus,
them are three-dimensional, however, and cannot be mapped for example, another mechanoreceptor on the thumb is much
simply into a two-dimensional cortex. The number of dimen- more likely to be responding simultaneously than a mech-
sions represented in M1 is arguably much more than three, if anoreceptor on the little finger. Some economy of neural
each muscle, each degree of freedom at each joint, and each
processing presumably is achieved by representing thumb
kinematic or dynamic parameter of movement constitutes a
mechanoreceptors close to one another, with little finger
possible dimension. Even in S1, the most discrete and well-
ordered somatotopic representation of the different fingers is mechanoreceptors represented at a distance. In the much
found in area 3b, where cutaneous inputs predominate less likely event that the thumb and little finger are indented
(Iwamura et al. 1983a; Pons et al. 1987). In areas 1 and 2, simultaneously, however, the requisite neural processing is
where cutaneous inputs are combined with inputs from deep more costly than if the thumb and little finger mechanore-
mechanoreceptors in joints and muscles, increasing numbers of ceptor representations were intermingled with one another.
receptive fields span multiple digits, and somatotopic organi- Control of movement, particularly the control provided by
zation becomes more complex, particularly in awake animals M1, is fundamentally different. Innumerable combinations of
(Iwamura et al. 1980, 1983b, 1993; Pons et al. 1985). In muscle contractions and movements with relatively similar
contrast, V1 represents additional dimensions by nesting them likelihood must be represented. In this way M1 provides the
within the two-dimensional retinotopic representation. Ocular capacity to generate a huge repertoire of movements, as well as
dominance columns, orientation columns, and color blobs can the potential to generate previously unperformed movements.
be considered additional dimensions of visual stimuli, the To achieve these abilities, the organizational substrate of M1
representations of which are nested within the two-dimensional must be able to access virtually any different combination of
representation of each retinotopic location. Little evidence of muscle contractions and body part movements with equal
such a fine-grained nesting has been found in M1, however, facility. A well-ordered, discrete, somatotopic representation
which presumably reflects some additional difference in corti- would limit its ability to do so. Such a well-ordered somato-
cal processing for control of movement versus perception of topic representation in M1 often has been likened to a piano
sensory stimuli. keyboard, on which other cortical areas play out movements, as
illustrated in Fig. 10A, where colors have been added to the
4
Indeed, the resolution of somatotopic organization in area 3b exceeds that white keys to identify individual notes. Although many differ-
which would be expected based on the divergence of thalamocortical afferents ent tunes can be played on such a keyboard, a 21st century
carrying somatosensory input from a given finger, and the overlap of thalamo- composer might be disappointed that certain combinations of
cortical afferents carrying input from different fingers (Garraghty et al. 1989;
Rausell et al. 1998). The precise somatotopy in area 3b therefore indicates that
notes simply cannot be played. For example, a single pianist
active mechanisms normally increase the somatotopic resolution in S1, in cannot play the five notes indicated by black dots in Fig. 10A.
contrast to the mechanisms organizing M1. If, however, a modern two-dimensional keyboard is created in

2140 M. H. SCHIEBER
which each note (white keys only for simplicity) is re-repre- therefore can be quite segregated in M1. Movements of the
sented at multiple locations (Fig. 10B), then at some location thumb and the wrist are not so independent. Extrinsic muscles
the desired combination of five notes can be accessed as easily acting on the thumb (flexor pollicis longus, extensor pollicis
as any other combination. Distributed organization thus can longus, and abductor pollicis longus) act across the wrist as
provide much more flexible access to a wide variety of com- well, and because the proximal segment of the thumb is con-
binations. nected to the wrist directly, motion of the thumb will exert
In theory, all possible combinations could be equally repre- interaction torques at the wrist. Precise control of thumb move-
sented. In practice, equivalent representation of all possible ment therefore will always require some control of the wrist,
combinations might come at the cost of an excessively large even when the wrist is being stabilized so as not to move when
cortical area. More area is required to re-represent any element the thumb does. Because movement of the thumb always
multiple times (compare the size of Fig. 10, A vs. B), and the requires some degree of simultaneous control of the wrist, then,
right connections must be established and maintained through- representation of the thumb and the wrist is intermingled to a
out a relatively large area, with relatively long conduction considerable degree in M1. Even more intermingled in M1 are
delays. A compromise therefore might exist in which more representations of thumb and fingers. Movements of the dif-
frequently used combinations are represented at more locations ferent digits are not entirely independent (Hager-Ross and
than less frequently used combinations. Hence when activated Schieber 2000; Schieber 1991). In functional uses of the hand,
by electrical stimulation, the extent of cortical territory repre- even when performing sophisticated tasks such as typing or
senting these frequently used combinations, and the corre- playing the piano, the thumb and fingers are in motion simul-

sponding body parts, would appear magnified relative to other taneously (Engel et al. 1997; Fish and Soechting 1992; Santello
less frequently used combinations and body parts. As the and Soechting 1998).
individual learns new motor skills (or quits practicing old ones) The need to control a wide variety of movements in biome-
such a distributed system (with the underlying structural sub- chanically coupled, simultaneously moving body parts may
strates of convergence, divergence, and horizontal interconnec- have constrained evolution of a well-ordered, spatially segre-
tion) could be reorganized to represent new combinations (at gated, discrete somatotopic map in M1. Indeed, when Hugh-
the expense of now less used combinations) more readily than lings Jackson initially proposed localization of control of
a well-ordered somatotopic system. movements in the brain, he recognized that, “. . . since the
Distributed organization also provides greater resistance to movements of the thumb and fingers could scarcely be devel-
the disruptive effects of lesions. A tiny lesion the size of a oped for any useful purpose without fixation of the wrist . . . ,
single piano key, for example, could eliminate any ability to we should a priori be sure that the center discharged, although it
produce a given note (such as the pale yellow E) in the might represent movements in which the thumb had the leading
well-ordered keyboard of Fig. 10A. The same tiny lesion would part, must represent also certain other movements of the forearm,
go virtually unnoticed in the distributed keyboard of Fig. 10B. upper arm, etc., which serve subordinately” (Jackson 1958, p. 69).
A considerably larger lesion covering many keys, would be
needed to noticeably compromise use of any given element on The author thanks J. Gardinier for preparing illustrations, M. Hayles for
the distributed keyboard. When such a lesion occurs, however, editorial comments, and the anonymous reviewers for helpful critiques.
This work was supported by National Institutes of Health Grants R01-NS-
use of many notes all along the musical scale would be com- 27686 and P41-RR-09283.
promised, consistent with the observations reviewed above that
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Constraints On Somatotopic Organization in The Primary Motor Cortex

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Constraints on Somatotopic Organization in the Primary

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FIG. 6. Divergence in the projection of single corticospinal neurons. A: a

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that the territory active during movements of multiple fingers

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FIG. 10. Cortical pianos. A: the standard

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