The Journal
of Neuroscience,
February
1994,
14(2):
630-644
Dynamic Construction
of a Neural Network from Multiple Pattern
Generators in the Lobster Stomatogastric
Nervous System
Pierre Meyrand,
Laboratoire
John Simmers,
de Neurobiologie
and Maurice
et Physiologie
Moulins
Compar6es,
Universitk
In the stomatogastric
nervous system (STNS) of the lobster
Homarus gammarus, the rhythmic discharge
of a pair of identified modulatory
neurons (PS cells) is able to construct
de
no~oa functional network from neurons otherwise
belonging
to other functional
networks.
The PS interneurons
are electrically coupled and possess endogenous
oscillatory
properties that can be activated synaptically
by stimulation
of an
identified sensory pathway. PS neurons themselves
project
synaptically
onto the three major neural networks
(esophageal, gastric mill, and pyloric) of the STNS. When a PS is
rhythmically
active in vitro, either spontaneously
(rarely) or
in response to direct stimulation,
it dramatically
restructures
the otherwise
independent
activity patterns of all three target
networks. This functional reconfiguration
elicited by a single
cell does not rely on changes in neuronal allegiance
to preexisting circuits, or on a simple merger of these different
circuits. Rather, PS is responsible
for the creation of an entirely new motor rhythm in that, via its widespread
synaptic
connections,
the interneuron
is able to subjugate the ongoing
activity of the three STNS circuits and selectively
appropriate individual
elements to its own intrinsic rhythm. In addition, PS excites motor neurons that innervate dilator muscles
of a valve situated between the esophagus
and the stomach.
The reorganization
of the regional foregut motor rhythms by
the interneuron
is therefore
coordinated
to the opening of
this valve, which itself carries sensory receptors
that have
been found to activate bursting in PS. Our data suggest that
the role of PS in massively restructuring
stomatogastric
output is to generate
a unique motor pattern appropriate
for
swallowing-like
behavior. In a wider context, moreover, the
results demonstrate
that a neural network may not exist as
a predefined
entity within the CNS, but may be dynamically
assembled
according
to changing
behavioral
circumstances.
[Key words: Crustacea,
stomatogastric
nervous system,
neural networks,
modulatory
interneuron,
bursting properties, network reconfiguration,
swallowing
behavior]
The CNS can be considered as an ensemble of neuronal networks, subsystems of interconnected
neurons that are each dedicated to a particular function. One type of neural circuit are
those responsible for rhythmic motor behaviors, so-called cen-
Received
Mar. 26, 1993; revised
July 8, 1993; accepted
July 15, 1993.
This work was supported
by the Human
Frontier
Science Program.
Correspondence
should
be addressed
to Dr. Pierre Meyrand,
Laboratoire
de
Neurobiologie
et Physiologie
Compar&es,
UniversitC
de Bordeaux
I and CNRS,
Place du Dr. Peyneau,
33120 Arcachon,
France.
Copyright
0 1994 Society
for Neuroscience
0270.6474/94/140630-15$05.00/O
de Bordeaux
I and CNRS, 33120
Arcachon,
France
tral pattern generators (CPGs) because of their intrinsic ability
to produce elemental output patterns in the absence of sensory
input (Delcomyn, 1980). In a number of preparations, especially
of simpler invertebrates
(Getting, 1989) the cellular and synaptic properties underlying
this endogenous rhythmicity
have
been investigated, and are now relatively well understood. It is
also now clear that in viva, individual
CPGs do not have a fixed
output but can assume different functional configurations
and
produce a variety of motor patterns according to sensory (e.g.,
Getting and Dekin, 1985; Bekoff et al., 1987; Katz and HarrisWarrick, 199 1) and central modulatory
inputs (Harris-Warrick
et al., 1992). While reinforcing the notion of the “polymorphic”
neural network (Getting, 1989) however, these studies have
remained within the conceptual framework of individual
CPGs
operating as more-or-less
discrete entities, each responsible for
the elaboration
of a specific, albeit flexible, motor behavior.
Recently, however, attention has become focused on a number of indications
that central pattern-generating
networks do
not always operate as structurally and functionally
independent
units, but can interact to produce complex and behaviorally
different changes in motor output. In vertebrates, for example,
different coordinations
of “unit” CPG circuits (Grillner,
198 1)
can produce behaviors as diverse as walking, running, swimming, and scratching (Grillner,
1985). In the lamprey spinal
cord, changes in coordination
of segmental rhythm generating
circuits can produce undulatory movements appropriate
for forward or backward swimming (Grillner,
199 l), while in Tritonia,
different combinations
of interacting
neurons result in swimming or a defensive withdrawal
response (Getting and Dekin,
1985). What neural processes underlie the network reorganization required for this level of behavioral flexibility?
In this respect, insight has been gained by recent cellular studies on the stomatogastric
nervous system (STNS) of Crustacea.
Although the four major rhythm-generating
circuits ofthe STNS
have been considered classically as separate functional entities
on the basis of their different neuronal composition,
activity
patterns, and the different muscle assemblages they control (Selverston and Moulins, 1987) it is now evident that these circuits
interact to a greater extent than previously
thought. For example, Hooper and Moulins (1989) demonstrated
that a single
pyloric neuron can switch its firing pattern from the pyloric to
cardiac sac networks, while neurons thought to be involved
exclusively in the generation of the gastric motor rhythm were
found able to participate
in pyloric network activity and vice
versa (Weimann et al., 199 1). In an another recent study, a bathapplied peptide was found to elicit a new rhythm in which the
cardiac sac and gastric networks were coordinately
active (Dickinson et al., 1990). In all three cases, however, the behavioral
significance of these internetwork
interactions
and the cellular
The Journal
of Neuroscience,
February
1994,
14(2)
631
STG
ivn
C
LG
VD
mvn
R
03w
RI
;
Figure 1. The STNS of the lobster, Homarus garnrnarus. A, Lateral view of the foregut showing the four different functional regions and the
STNS in situ. Anterior is toward the left. B, Schematic representation of the STNS after isolation. C, Simultaneous extracellular nerve recordings
showing typical spontaneous motor output of the different STNS networks in vitro. B, brain; COG, commissural ganglion; C’S, cardiac sac; G. Mill,
gastric mill; LG, lateral gastric motor neuron; OCSV, esophageal cardiac sac valve; OE, esophagus; OG, esophageal ganglion; 03n, esophageal
nerve 3 containing dilator ODl (largest unit) and constrictor OC (smallest unit) motor neurons; P, pyloric chamber; STG, stomatogastric ganglion;
VD, ventral dilator motor neuron; agn, anterior gastric nerve; ivn, inferior ventricular nerve; Ivn, lateral ventricular nerve; mvn, median ventricular
nerve; stn, stomatogastric nerve; vpon, ventral posterior esophageal nerve.
pathways that might govern them in vivo remain unknown.
Importantly
moreover, in these examples the structural and
functional integrity of each original network is essentially maintained. Thus, the possibility that individual
neurons are able to
participate
in behaviors other than those generated by preexisting neuronal circuitry was not addressed.
In the present study, we have investigated the global reorganization
of lobster stomatogastric
networks induced by the
rhythmic discharge of a pair of identified interneurons.
We find
that these neurons, originally located and named “pyloric suppressor” (PS) neurons on the basis of their inhibitory
influence
on the bursting properties of certain pyloric neurons (Cazalets
et al., 1990a,b), are able to reconfigure the different STNS networks into a new functional circuit that bears no resemblance
to any of the original networks. This de novo network construction relies on the capacity of PS to override selectively the synaptic and cellular events responsible for the generation of the
pyloric, gastric, and esophageal rhythms, and to recombine certain of these elements into a new network that is active in time
with interneuron’s
own endogenous bursting. We have also examined the effects of PS on other STNS motor output, as well
as its control by sensory input pathways. Our results lead us to
conclude that PS is intimately
involved in organizing and driving a hitherto undescribed
foregut motor activity, namely, that
underlying swallowing-like
behavior.
Preliminary
reports of some of these data have appeared
(Meyrand et al., 199 1; Simmers et al., 199 1).
Materials and Methods
All experiments (n = 75) were performed on the European lobster,
Homarus gammarus, obtained from local fishery supply. The animals,
weighing 300-400 gm, were maintained in the laboratory in large tanks
of aerated circulating seawater at 14°C.
Electrophysiology. Two types of in vitro preparation were used in
electrophysiological experiments reported here.
(1) The completely isolated stomatogastric nervous system (STNS;
see Fig. 1) using standard dissection and recording procedures described
previously (Selverston and Moulins, 1987). The stomatogastric ganglion
(STG), commissural ganglia (COG), and the proximal part of the inferior
ventricular nerve (ivn), which contains the somata of the PS neurons,
were desheathed to allow access for intracellular recordings, while the
activity of individual nerves was monitored extracellularly with monopolar platinum wire electrodes.
(2) A nervous system-muscle preparation consisting of the STNS left
attached to the foregut after the latter had been removed from the animal
and opened along the ventral midline. After pinning out on a Sylgardlined petri dish, the PS neurons were recorded intrasomatically in the
ivn, while a second microelectrode was used to record from individual
fibers of selected foregut muscles.
The physiological saline used to bathe both types of preparation consisted of (in mM) 479 NaCl, 12.74 KCl, 13.2 CaCl,, 10 MgSO,, 3.9
Na,SO,, 5 HEPES, and adjusted to pH 7.45 with HCl or NaOH. The
preparations were continuously superfused with saline held at constant
temperature (12-l 4°C) with a laboratory-constructed
thermoelectric
632
Meyrand
et al. * Functional
Reconfiguration
of Multiple
Neural
Networks
son
lmm
Figure 2. Morphological and electrophysiological identification of the PS
neurons. A, Camera lucida drawing of
one PS neuron after injection of HRP.
B, Schematic representation of PS in
the STNS showing its soma location in
the inferior ventricular nerve (ivn), and
axonal processes. C, Four superimposed oscilloscope sweeps triggered by
PS spikes recorded intrasomatically.
Each action potential in the soma is followed at constant latency by an extracellular spike in the superior esophageal
(son) and stomatogastric (stn) nerves.
Ll-F, Each PS spike elicits a constantlatency EPSP in pyloric motor neuron
VD in the STG (D, three sweeps),
esophageal constrictor motor neuron
OC in the COG (E, six sweeps), and the
left and right commissural gastric intemeurons (CC/, CGr) in the COGS (F,
four sweeps). ion, inferior esophageal
nerve; on, esophageal nerve; son, superior esophageal nerve. See Figure 1
for other abbreviations. Calibration (CF): 5 mV, 10 msec.
C
stn
son
PS
D
F
CGI
VD
-1
CGr
PS
cooling system. Glass micropipettes filled with 3 M KC1 (resistance of
10-20 MO) were used for both neuron and muscle recordings. World
Precision Instruments electrometers were used for intracellular recordings and current injection, while extracellular recordings were made
with Grass amplifiers. Signals were displayed on a 5 113 Tektronix oscilloscope, stored on an MP 552 1 Schlumberger magnetic tape recorder,
and transposed on paper with a Gould ES 1000 electrostatic recorder.
In experiments where the PS cell bodies were not impaled with a
microelectrode (as in Figs. 7 and 9B), the intemeurons were stimulated
extracellularly with a wire electrode placed carefully on the proximal
region of the desheathed ivn, between their somata and the esophageal
ganglion (see Fig. 2B).As established previously (Cazalets et al., 1990a),
the effects of stimulating the ivn in this region derive solely from the
activation of the PS neurons since identical stimulation of remaining
ivn fibers (by placing the electrode at points more distal to the PS somata)
has no effect on STNS activity. Moreover, we verified that all STNS
responses to extracellular stimulation of the proximal ivn were seen in
other preparations where PS was activated by direct intrasomatic current
injection.
Morphology.To visualize the axonal projections of PS, horseradish
peroxidase (HRP; 10% in 0.2 M KCl) was iniected into one or both PS
neurons by‘applying brief (250 msec) pressure pulses (15 psi) with a
Picospritzer coupled to the back of an intrasomatically placed microelectrode. Injection times ranged from 30 min to 1 hr, and then the
preparation was left for 24 hr at 13°C to allow maximum dye migration.
The preparation was then exposed to the HRP substrate 3,3’-diaminobenzidine tetrachloride (1.5 mg/ml; Sigma) to produce a brown reaction product in the injected neuron(s), and standard procedures were
subsequently employed to fix, clear, and draw the stained cell in situ
under light microscopy. In some experiments, PS somata were injected
iontophoretically with 3% Lucifer yellow CH (Sigma) and then the neurons were processed and viewed with an epifluorescent microscope,
again using conventional methodology.
Results
Multiple network activity of the STNS in vitro
The foregut of large crustaceanssuch as lobsters and crabs is
divided into two main regions,a short esophagus(Fig. IA, OE)
and a large stomach separatedby a sphincter, the esophageal
cardiac sac valve (OCSV). The stomach itself is divided into
three anatomically and functionally distinct compartments;the
The Journal
cardiac sac (CS), gastric mill (G. Mill), and pyloric chamber(P)
(Fig. 1A). As described originally (Maynard and Dando, 1974)
each region is controlled by a specific set of muscles that are
innervated by the STNS.
When isolated from the crustacean foregut, the STNS (Fig.
1B) spontaneously produces the separate rhythmic motor patterns that underlie the different regional behaviors of the foregut
in vivo (Fig. 1C, Rezer and Moulins, 1983; Heinzel, 1988). The
esophageal rhythm consists of alternating bursts of impulses in
the esophageal dilator and constrictor motor neurons occurring
at a cycle period of 4-6 set (Spirito, 1975). The somata of
esophageal motor neurons lie either in the esophageal ganglion
or the bilateral commissural ganglia (see Fig. lB), and their main
role is to generate peristaltic movements that move food up the
esophageal tract from the mouth toward the cardiac sac region
of the stomach (Fig. 1A). In spiny lobsters (Palinurus vulgaris
and Panilurus interruptus), motor neurons innervating the cardiac sac region are also involved in a discrete rhythm that operates at cycle periods of between 20 and 60 set (Moulins and
Vedel, 1977; Vedel and Moulins, 1977; Dickinson and Marder,
1989). In our in vitro preparations of the European lobster Homarus gammarus, however, we have never observed cardiac saclike activity either arising spontaneously or in response to neuronal stimulation (see below). Caudal to the cardiac sac ‘is the
gastric mill system (Fig. lA), consisting of two lateral teeth and
a single medial tooth that act in combination to shred and chew
ingested food (Heinzel, 1988). The period of the gastric rhythm
is between 5 and 10 set and the somata of all gastric motor
neurons are located in the STG ganglion (Maynard, 1972). The
most caudal region of the foregut consists of the pyloric chamber, which serves to move food from the stomach to the midgut.
The movements of the pyloric region are controlled by a welldescribed neuronal network (Miller, 1987) also contained in the
STG ganglion and producing the fastest STNS rhythm with a
period of l-2 sec.
In Homarus gammarus, we find patterns of activity and neuronal organization of the networks generating the three main
STNS rhythms that are very similar to those described in other
species. Figure 1C shows simultaneous extracellular recordings
of typical spontaneous activity in pyloric, gastric, and esophageal motor neurons. Here gastric activity was monitored by the
lateral gastric motor neuron (LG) recorded from its axon in the
medial ventricular nerve (mvn), pyloric rhythmicity by the ventral dilator motor neuron (VD) also carried in the mvn, and
esophageal output by esophageal nerve 3 (03n), which contains
both dilator (ODl) and constrictor (OC) motor neurons.
Although the different STNS circuits underlying these regional
foregut activities can generate basal rhythms in the absence of
sensory feedback as seen in Figure 1C, they are normally subject
to an array of modulatory influences that shape motor output
to the behavioral needs of the animal. A wide range of neureactive substances appear to play a modulatory role within the
STNS (Marder, 1987) and several central neurons that modulate these networks have now been identified in various species
(Harris-Warrick
et al., 1992). Among these identified input neurons is a pair of cells that were previously found in Homarus
(Cazalets et al., 1990a) and named pyloric suppressor (PS) on
account of their apparent inactivating influence on rhythmic
motor output from the pyloric network (Cazalets et al., 1990b).
However, as described in the remainder of this report, the PS
interneurons not only project onto the pyloric network but also
exert dramatic effects on the other STNS networks.
of Neuroscience,
February
1994,
74(2)
633
1
PSI
-
I
ps2-7Y-1
i
1
I
I
z---L
-I
3. The two PS neurons are electrically coupled. Depolarization
(I) or hyperpolarization (2) of one PS (PS2) by current injection (i)
causes depolarization or hyperpolarization of its uninjectedpartner (PSI).
Similar responses are obtained in PS2 (3) and (4) by manipulating the
membrane potential of PSI. Calibration: 5 mV (current 5 nA), 1 sec.
Figure
Location, axonal projections, and endogenous properties of PS
cells
In Homarus gammarus, the somata of the two PS intemeurons
are contained in the ivn, which directly connects the brain to
the STNS (Fig. 2A,B), located side by side within S-10 mm of
the ivn’s point of entry into the esophageal ganglion. Morphological and electrophysiological approaches reveal a complex
axonal geometry of the PS cells. First, direct intrasomatic injection of HRP demonstrates that both PS neurons send branches into the five main rostra1 nerves of the STNS, confirming the
earlier observations of Cazalets et al. (1990a), who used cobalt
backfills of whole nerve tracts. A single process arising from the
monopolar soma descends in the ivn toward the esophageal
ganglion, where it splits into three branches (Fig. 2A,B). The
medial branch reaches the son/stn junction nerves via the esophageal nerve (on), while the other two branches pass laterally into
the left and right ions and project toward each commissural
ganglion. Important to note is that with either HRP (Fig. 2A)
or Lucifer yellow injections (not shown), dendritic ramifications
or neuropilar processes of PS were never seen in the OG. From
the son/stn junction each PS neuron sends axon branches into
both sons and the stn, a geometry that is confirmed electrophysiologically in Figure 2C, which shows spontaneous intrasomatic spike activity of a PS neuron recorded along with an
extracellular monitor of the stn and the bilateral sons. Each soma
spike of PS is followed 1: 1 and at constant latency by an axonal
impulse in the son and eventually the stn. By contrast, we have
never detected extracellular spikes of PS in the ions, nor is it
possible to elicit impulses in the soma with direct ion electrical
stimulation (see also Cazalets et al. 1990a), suggesting that the
projections of PS in the ions are unable to support action potentials.
As suggested by the morphological and physiological data of
Figure 2, A and C, the branches of each PS serve to distribute
the cell to the different stomatogastric ganglia. The widespread
nature of the neuron’s synaptic connectivity is illustrated in
Figure 2Ll-F, where each intrasomatically recorded action potential in PS is followed at constant latency by an EPSP in a
634
Meyrand
et al. - Functional
Reconfiguration
of Multiple
Neural
Networks
A
PS
Figure 4. Oscillatory burst-generating
membrane property of PS neurons. A,
Intracellular recording of a PS cell during an episode of spontaneous rhythmic
activity. Note the ramp-like depolarization underlying each spike burst and
a lack of discrete synaptic activity. B,
The frequency of oscillation and bursting is voltage dependent. Continuous
depolarization of PS with intrasomatic
current injection increases the frequency of oscillation as a function of current
(l-3 nA). C, Resetting of ongoing
rhythmic activity in PS (elicited by continuous depolarizing current injection)
by a brief (250 msec) hyperpolarizing
pulse (2.5 nA) injected into the cell. Arrowsabove record indicate the expected
time of burst termination in the absence
of perturbation. Calibration: 10 mV, 2
sec.
pyloric neuron, the VD located in the STG ganglion (Fig. 20)
an esophagealconstrictor motor neuron (OC) in one commissural ganglion (Fig. 2E), and each of the singlebilateral pair of
commissuralgastric interneurons (CG; Simmersand Moulins,
1988) located in the two commissuralganglia (Fig. 2F). Thus,
PS makesoutput connections in the STG and bilaterally symmetrical connections in the left and right COGS(Fig. 2B).
No qualitative differences in axonal geometry and synaptic
connectivity of the two PSneuronshave beendetected, and this
apparent equivalence is further indicated by the finding that the
two cells are electrically coupled. As evident in Figure 3, where
both PS neurons were recorded simultaneously, injection of
depolarizing current into the cell body of PS2 (Fig. 3, panel 1)
or PS1 (panel 3) causeda depolarization, without delay, of PS1
and PS2, respectively. Conversely, an hyperpolarizing pulse of
current injected into either PS2 (Fig. 3, panel 2) or PSI (panel
4) causedhyperpolarization of the other neuron. The outcome
of this electrical coupling, therefore, is that when active the two
neurons will tend to operate in synchrony and behave as a
functional unit.
Although the PS neurons are generally silent in our in vitro
preparations, they very occasionally expressbouts of spontaneousrhythmic activity, which consistsof oscillationsin membrane potential underlying intense bursts of action potentials
(Fig. 4A). This rhythmic activity doesnot appear to arise from
a discretesynaptic drive but rather, and as evident in Figure 4,
B andeC, it appearsto be due to an endogenousburst-generating
mechanism.First, when PS is silent, the injection of sustained
depolarizing current into the somainvariably elicits oscillatory
activity (Fig. 4B) consisting of repetitive ramp-like depolarizations (pacemaker potentials) that drive rhythmic bursting.
Second, the frequency of these current-induced oscillations is
voltage dependentin that beyond a discreteactivation threshold,
an increasein the level of tonic depolarization (1, 2, 3 nA; Fig.
4B) is associatedwith a correspondingincreasein rhythm frequency. Third, and consistentwith a further classicaltest of an
endogenousoscillator (Pinsker, 1977), it is possibleto resetthe
rhythmic activity ofPS neuronswith experimental perturbation.
In the recording of Figure 4C, for example, where PS was held
tonically depolarized to elicit bursting, an additional brief hyperpolarizing pulse delivered during a cycle of PS activity terminated prematurely the corresponding spike burst and permanently reset the cell’s ongoing rhythm (seearrows above
records in Fig. 4C). From these observations, therefore, we
conclude that the oscillatory capability of the PS neuronsis an
inherent membraneproperty of the interneurons themselves.
Injluence of PS on STNS neural networks
Given the widespread synaptic connections and endogenous
burst-generatingproperties of PS, an obvious initial question is
whether theseinterneurons are implicated in generatingthe different motor rhythms of the foregut. However, that this is not
the casecan be seenin Figure 54 (seealsoFig. 1C), which shows
simultaneousintrasomatic recordingsfrom a ventricular dilator
(VD) motor neuron of the pyloric network, a constrictor motor
neuron (OC) of the esophagealnetwork, and the medial gastric
The Journal
of Neuroscience,
February
1994,
14(2)
636
Figure 5. The PS neurons are not necessary for generation of the different STNS motor patterns. A, Simultaneous intracellular recordings from
pyloric (ventral dilator, VD), esophageal (esophageal constrictor, OC), gastric (median gastric, MC) and PS neurons showing their respective
spontaneous output patterns although PS is silent. B, PS does not drive the cardiac sac rhythm generation as revealed by an intracellular recording
from a cardiac sac neuron (cardiac dilator 1, CDI) during an episode of rhythmic PS firing elicited by tonic depolarizing current. Calibration: 15
mV, 2 sec.
(MC) motor neuron of the gastric network. In this experiment,
a fourth microelectrode monitored PS, which remained inactive
throughout the recording sequence illustrated. Evidently, therefore, spontaneous and robust expression of each of these three
separate STNS networks has no reliance upon the discharge of
interneuron PS.
A second possibility is that the PS neurons act as pacemakers
for the cardiac sac rhythm, in a manner homologous to the ivn
cells that drive cardiac sac activity in the spiny lobster Palinurus
(Moulins and Vedel, 1977). Our inability to observe a distinct
cardiac sac rhythm in in vitro preparations of Homarus and the
rarity with which PS itself is spontaneously active are consistent
with this notion. However, as seen in Figure 5B, PS does not
appear to be the driver of the cardiac sac rhythm. In this experiment, cardiac dilator motor neuron CD1 was monitored
intracellularly in the esophageal ganglion while a penetrated PS
neuron was held tonically depolarized to elicit rhythmic bursting. Despite intense bursts of discharge in PS, however, CD1
and other cardiac sac motor neurons (not shown) remain weakly
active with little evident relationship with the firing of the intemeuron.
The synaptic connections of PS with neurons belonging to the
pyloric (Cazalets et al., 1990b), gastric, and esophageal networks
(Simmers et al., 199 1; see also Fig. 2C-E) suggested that, when
active, the interneuron must at least have an influence on the
ongoing activities of these three independent networks. To test
for such effects we recorded simultaneously from neurons belonging to the different STNS networks when PS was active. In
Figure 6, for example, the output of the pyloric and gastric
networks was monitored via the axons of VD and LG in the
mvn, while the esophageal network was monitored by recording
the 03n nerve, which contains the axon of an esophageal dilator
motor neuron (ODl). When PS was silent (Fig. 6A; also see Fig.
SA) these three networks again can be seen to be spontaneously
active at characteristic and unrelated cycle frequencies, with the
pyloric rhythm (see VD bursts) being the fastest and the gastric
rhythm (see LG) the slowest pattern. However, when PS becomes active, as in Figure 6B where bursts were elicited by
repetitive depolarization of the cell, a dramatic alteration in
these independent motor patterns occurred whereby they now
become closely coordinated to the discharge of PS. First, the
esophageal dilator neuron in 03n is strongly activated during
636
Meyrand
A
et al. + Functional
Reconfiguration
of Multiple
VD
Neural
Networks
LG
mvn
03n
PS
I
i
Figure 6. Influence of PS discharge on extracellularly recorded STNS motor patterns. A, A PS cell monitored intracellularly along with the pyloric
and gastric rhythms recorded extracellularly from the motor nerve (mvn) that contains the axons of pyloric VD and gastric LG neurons, and the
esophageal rhythm monitored from the dilator ODl neuron in the esophageal 03 motor nerve. When PS is silent the three motor networks express
their characteristic and independent patterns. B, Alteration in these separate patterns during bursts in the same PS elicited by repetitive depolarizing
current pulses. Pyloric VD and gastric LG neurons are now coordinated, with VD firing late in the phase of PS discharge and in antiphase with
LG. The frequency of the esophageal rhythm is also strongly increased during each PS burst. Calibration: 10 mV, 2 sec.
PS discharge,firing rhythmic multiple bursts in time with each
interneuronal burst. Second, the pyloric (VD) and gastric (LG)
neurons,which normally operateat completely different periods
(Fig. 64, now burst in strict time with the PS cycle (Fig. 6B),
with VD firing prolonged bursts in phasewith the dischargeof
PS while LG is active in antiphase with the interneuron.
Theseprofound changesin STNS network activity during the
dischargeof PSare further evident in Figure 7, where individual
members of the pyloric and gastric circuits were recorded intracellularly. Figure 7A showsthe typical independent activity
of these networks, here monitored by neurons PD and LPG,
respectively, when the PS neurons were silent. However, repetitive high-frequency (50 Hz) spike trains (duration of 5 set)
in PS elicited by direct electrical stimulation of their axons in
the ivn (Fig. 7B,C, seeMaterials and Methods) coordinate the
two elementsinto a singlerhythm that is completely unrecognizable from either the original pyloric or gastric rhythms, but
which is again coupled to the dischargeof PS. Motor neuron
PD is strongly depolarized at the onset of PS firing and repolarizes immediately when PS falls silent, and although the cell
continues to receive pyloric-like rhythmic synaptic excitation
in the interval betweeneachPSburst, it remainssilent until the
interneuron is once again active. Gastric neuron LPG is also
powerfully excited during PS discharge, but with a retarded
depolarizing responsethat far outlasts the interneuron’s own
duty cycle. Therefore, despite thesetemporal differencesin the
responsesof individual neurons,the first conclusion from these
data is that PSis able to completely reorganize ongoingactivity
of otherwise independent STNS circuits to produce a single
conjoint rhythm consisting of elements firing more or lessin
phase(e.g., VD, Fig. 6; PD, Fig. 7) biphasically (e.g., LPG, Fig.
7) or in antiphase(e.g., LG, Fig. 6) with the interneuron’s own
dischargepattern. Moreover, the strict dependenceof this reorganized pattern on PS activity is evident in Figure 7, B and
C, where repetitive stimulation of the PS axons was made at
two different cycle periods. In both cases(compare Fig. 7, B
and C) the new conjoint pattern remained closely timed to the
burst frequency of PS.
These dramatic effects of PS do not merely consist of an
overall appropriation of each STG circuit to the interneuron’s
own firing pattern, but rather involve selectiveand very different
influenceson individual neuronsof each circuit. This diversity
in the action of PSis illustrated in Figure 8, where motor output
from the pyloric network is monitored by two of its integral
members, the VD and LP neurons. When the penetrated PS
interneuron is inactive or firing at low frequency, the two pyloric
elementsexpresssimilar and coordinated oscillatory behavior
typical of pyloric rhythmicity in vitro (Fig. 8, left). However,
when PS itself starts to fire rhythmically (here evoked by continuous intrasomatic depolarization), pyloric activity is immediately disrupted with the neuron VD now firing prolonged
bursts in phase with each PS burst. In contrast, neuron LP
The Journal
of Neuroscience,
February
1994,
14(2)
637
PD
LPG
PS
C
7. Rhythmic discharge of a PS neuron restructures independent stomatogastric motor outputs into a single pattern timed to the intemeuron’s
own rhythm. A, Spontaneous rhythmic activity of the pyloric and gastric networks monitored intracellularly from pyloric (PD) and gastric (LPG)
neurons in the absence of PS firing. B and C, Repetitive spike trains in PS elicited by extracellular axonal stimulation of the proximal ivn (5 set
trains at 50 Hz; PS traces are direct monitors of stimulation) completely alters the activity of these neurons, which are now coordinated in a single
rhythm timed to the firing of PS whatever the stimulus period. The PD neuron is strongly depolarized in phase with PS firing while the LPG neuron
receives delayed excitation and continues to fire after each PS burst. Calibration: 10 mV, 2 sec.
Figure
638
Meyrand
et al. * Functional
Reconfiguration
of Multiple
Neural
Networks
VD
LP
PS
i +lnA
Figure 8. Rhythmic discharge of PS interneuron is able to dismantle the pyloric network. During a spontaneous pyloric rhythmicity (left), here
causes an immediate disruption
monitored by the VD and LP neurons, PS bursting elicited by tonic intrasomatic current injection (at arrowhead)
of the ongoing
and fires in phase with PS firing while LP hyperpolarizes and remains completely
- -_.~vloric -nattem: VD is now rhvthmicallv, denolarized
silent. Calibration: 10 mV, 1 sec.
hyperpolarizes to a relatively steady membrane potential and
remains completely inactive throughout the entire episode of
PS activity. This demonstrates that PS is not just able to coordinate the activity of elements originating from different STNS
networks as seen in Figures 6 and 7, but can functionally dismantle the individual circuits, discarding certain constituent
neurons (e.g., LP of the pyloric network in the example of Fig.
8) while recruiting remaining cells (e.g., VD in Fig. 8) to create
an entirely new motor pattern.
In addition to these effects seen during PS firing, we also
examined whether the interneuron has long-term influences that
outlast its own discharge. Following an episode of PS firing, the
recovery of original STNS network activity occurs in two ways.
First, the esophageal network, which controls motor activity of
the foregut region rostra1 to the OCS valve and is strongly activated by PS bursts, returns immediately to original levels of
activity when the interneuron falls silent (Fig. 9A). Second, and
in contrast to the esophageal pattern, neurons ordinarily belonging to the gastric and pyloric networks (which control movements of the foregut posterior to the OCS valve) remain coordinated in a single pattern that can persist for some considerable
time after the end of an episode of PS activity. As illustrated in
Figure 9B1, prior to PS discharge, neurons PD and GM can be
seen to participate in the two separate rhythms of the pyloric
and gastric networks, respectively. However, after a single 10
set burst in PS (not shown) these previously independent elements remain coordinated in a single motor pattern (Fig. 9B2)
with a cycle period that is different from either the original
pyloric or gastric patterns (compare with Fig. 9BI). This unified
pattern (in which the PD neuron is unable to express its faster
intrinsic pyloric period) persists for several tens of seconds, and
as seen in Figure 9B3, the recovery oftotally independent pyloric
and gastric network activity was still not complete some 3-4
min after the discharge of PS.
PS neurons drive dilation of the esophageal-cardiac sac valve
In addition to restructuring rhythmic movements normally
driven by the three STNS circuits as described above, PS also
influences other foregut muscles that are not directly controlled
by these networks. Examination of STNS-muscle preparations
(see Materials and Methods) revealed that one such set of mus-
cles is that controlling the valve situated between the esophagus
and the cardiac sac (Fig. 1A). The anatomy of the OCS valve
and its associated muscles in Homarus gammarus (Fig. lOA1,2)
were previously reported by Robertson and Laverack (1979)
who described three extrinsic dilator muscles (OCSVI-3) that
open the valve, while contraction of the single intrinsic constrictor muscle (OCSVC) causes the valve to close. The motor
neurons that innervate these muscles originate in the commissural ganglia.
In STNS preparations with the anterior part of the foregut
left attached, simultaneous intracellular recordings from a PS
neuron and muscle fibers of the OCS valve (Fig. 10B) show that
when the interneuron is inactive, motor neurons to the dilator
(OCSV3a) muscle remain silent while constrictor motor neurons
are spontaneously active, as evident from the continuous barrage of excitatory junction potentials in the OCSVC muscle.
Under these conditions, therefore, the OCS valve remains closed,
despite ongoing esophageal, gastric, and pyloric rhythmicity (not
shown). However, when PS becomes active (Fig. 1OB) the dilator
motor neurons are now excited, constrictor motor activity ceases, and the valve opens until shortly after the interneuron again
falls silent. Moreover, when PS fires rhythmically, whether spontaneously or in response to tonic depolarization (Fig. lOC), the
OCSV3a muscle (and hence valve dilation) is driven cyclically
in time with the interneuron’s own spike bursts, again for as
long as the latter remains active.
Although the PS interneurons appear to be intimately involved in driving OCS valve dilation as well as causing a massive restructuring of other STNS motor rhythmicity, the cells
are very rarely spontaneously active in our in vitro preparations.
We were therefore interested in whether PS themselves are subject to synaptic input that might govern their endogenous bursting capability in vivo. One discrete afferent pathway found to
influence PS is that shown previously to arise from a bilateral
set of sensory neurons (posterior esophageal sensors, pos), presumed chemoreceptors, located on the internal wall of the OCS
valve and which send their axons to the commissural ganglia
via the left and right ventral posterior nerves (vpons) (Robertson
and Laverack, 1979) (see Fig. 11A). That these sensory elements
have synaptic access to the active membrane properties of PS
is indicated in Figure 11B, where a brief electrical stimulation
The Journal
of Neuroscience,
February
1994,
f4(2)
639
PS
Bl
Before
PS discharge
GM
PD
B2
5 to 40s after
PS discharge
Figure 9. Short- andlong-termeffects
of PS neurons on stomatogastric network activity. A, Simultaneous intracellular
B3
3 to 3.5 min after
PS discharge
(10 msec) of either the left or right pos nerve distal to its entry
into the corresponding
vpon is able to trigger a long-lasting
(5
set) “plateau”
depolarization
in an otherwise silent PS interneuron, during which the cell fires at high frequency. This initial
indication
that these bilateral sensory pathways may play a
physiological
role in controlling
PS is further substantiated
by
their ability to initiate and maintain oscillatory bursting activity
when stimulated tonically (Fig. 11C). With onset of such stimulation, a previously inactive PS neuron depolarizes until it
reachesthreshold for endogenousoscillation and bursting, which
is then expressedthroughout the period of stimulation (Fig.
11C). From theseobservations, we conclude that synaptic excitation
mediated
by pos axons can activate
and sustain the
recordings
of an
esophageal
constrictor neuron (OC) and a PS intemeuron. Discharge of PS, elicited by
a depolarizing (1 nA) current pulse (note
bridge circuit unbalanced), induces an
increasein burstingfrequencyof OC
but the latter reverts immediately to its
initial frequency at the end of PS firing.
B, Simultaneous recordings from neurons of the gastric (GM) and pyloric
(I’D) networksbeforeand after PS discharge (10 set burst at 25 Hz; not
shown). Before PS discharge (BI) the
gastric andpyloricnetworksexpress
two
independent output patterns but immediatelyafter PS discharge(elicited
by axonal stimulation at 25 Hz for 10
set) the same neurons remain coordinated in a single motor pattern (B2) that
gradually weakens but remains evident
some 34 min later (B3). Calibration:
15 mV, 2 sec.
intrinsic bursting capability of PS and, as a consequence, elicit
rhythmic dilations of the OSC valve from which they arise.
Discussion
Our resultsshowthat the activity of a pair of electrically coupled
modulatory inter-neurons(PS) can completely reorganize the
different neuronal networks of the STNS and using elementsof
these otherwise independent networks construct a new functional network. We have shown that theseinterneurons, which
appearto be endogenousoscillators, alsodrive motor output to
a small set of foregut musclesnot directly implicated in the
activity patterns of these other STNS circuits. Moreover, the
interneurons can be activated by electrical stimulation of axons
640
Meyrand
et al. - Functional
Reconfiguration
of Multiple
Neural
Networks
A2
Al
Figure 10. The PS neurons control the
dilation of the OCS valve between the
esophagus and cardiac sac. A, Illustration of the OCS valve and muscles. Al,
Left lateral view. A2, Frontal view. B,
Simultaneous intracellular recordings
of constrictor (OCSVC) and dilator
(OCSI’3u) muscle fibers of the OCS
valve and a PS neuron. Depolarization
of PS by current injection (i) causes a
depolarization of the dilator fiber
(OCSV3a) due to a summation of excitatory junction potentials and inhibition of spontaneous tonic firing in
motor neurons to the constrictor muscle (OCSVC). C, Rhythmic bursting of
PS (elicited by current injection) drives
phase-locked depolarizations in the dilator muscle of the OCS valve. CS, cardiac sac; 03, esophagealdilator muscle
3; OCSVl-3, esophageal cardiac sac
valve dilator muscles l-3; OCSVC,
esophageal cardiac sac valve constrictor muscle; OE, esophagus. Calibration
(B and C): 10 mV, 1 sec.
OCSV3a
-L
PS
i
I
1
I--
C
OCSV3a
from a previously identified group of chemosensors located in
the internal esophageal wall. The reorganizing influence of PS
on the different STNS networks and its possible behavioral consequences are summarized in Figure 12.
Swallowing-like
activity in lobster
Although we do not know how the PS interneurons behave in
the intact animal, our in vitro data lead us to predict that these
two neurons control swallowing-like
behavior. When PS is active, its rhythmic bursting drives motor output for opening the
OCS valve (Fig. 10) and concomitantly reorganizes all other
foregut motor activity so that it becomes coordinated with these
movements (Figs. 6-8, 12). During opening of the valve, PS
strongly increases the frequency of the esophageal rhythm (Fig.
6B) and causes intense bursting, especially in esophageal constrictor motor neurons (Fig. 94. The functional consequence
of this effect in vivo is that it serves as the primary act in food
transit whereby particles are pushed through the now open valve
from the esophagus to the stomach. At this time, the neural
networks controlling foregut regions that are posterior to the
OCS valve are also altered by the discharge of PS in a manner
that would facilitate the rearward passage of food. For example,
the pylorus is dilated in phase with each valve opening via the
strong activation of dilator motor neurons (e.g., VD in Figs. 6B,
8) and the complete suppression of activity by the LP constrictor
motor neuron. In addition, masticatory movements of the three
gastric mill teeth in the stomach cavity are reorganized so that
power-stroke movements are either inhibited completely (Meyrand et al., 1991) or timed to occur in phase opposition with
each valve dilation (e.g., LG in Fig. 6B). The functional significance of the coordinated gastropyloric activity that is seen to
follow PS discharge (Fig. 9B) is less easy to predict, although
presumably this serves in a final mixing process before the gastric and pyloric circuits reassume their separate regional behaviors.
Sensory activation of feeding-related behavior
In Homarus gammarus, Robertson and Laverack (1979) first
reported a group of sensory cells, the posterior esophageal sensors (pas), located on the internal wall of the OCS valve, and
that when subjected to direct application of Mytilus extract in
semi-intact preparations, caused a powerful enhancement of
The Journal
A
of Neuroscience,
February
1994,
14(2)
641
Bl
PS
I
Stim
pas,
B2
Stim
pos,
C
PS
lllllll1l~
( ,‘/I
Stim
pos,
/
” ull u
10Hz
Figure II. Sensory activation of PS neurons. A, Schematic representation of the rostra1 end of the STNS in vitro showing the bilateral nerves
(upon, and vpon,) that carry the axons of the left and right posterior esophageal sensors @OS), chemoreceptors in the internal wall of the OSCV
valve, to the corresponding COG. B, A brief electrical stimulation (30 Hz for 250 msec) of the left (BI) or right (B2) pos axons triggers a longlasting depolarization in the same PS neuron. C, A tonic stimulation (10 Hz) of the nerve branch from the right pos in a different preparation
elicits phasic bursting activity in a PS neuron for the duration of the stimulation. vpon, ventral posterior esophageal nerve. See Figure 1 for other
abbreviations. Calibration: 10 mV, 2 sec.
esophageal peristalsis. Although
the effects of these presumed
chemoreceptors
on other foregut activity patterns were not investigated in their in vivo experiments, our in vitro data obtained
with axonal stimulation
of pos suggest that the motor responses
observed by Robertson and Laverack (1979) constituted one
component
of a far more complex behavioral
alteration
involving all foregut regions and mediated uniquely by the PS
interneurons.
Tonic activation from sensory feedback, and especially that
arising from chemoreceptors,
has been found to play a crucial
role in initiating
and sustaining feeding-related
behaviors in a
number of different preparations.
In the snail Lymnaea stagnalis, for example, a single interneuron
that is able to initiate a
feeding rhythm in quiescent isolated preparations
(Kemenes et
al., 1986) can be activated by chemical stimuli applied to the
lips (Rose and Benjamin,
198 la,b). In the carnivorous
marine
mollusk Pleurobranchea,a population
of interneurons
are excited by food extracts applied to rhinophores
and their discharge
also triggers fictive feeding behavior in a previously quiescent
preparation
(Gillette et al., 1982), while similar observations
have been made in Limax (Delaney and Gelperin, 1990a,b) and
Aplysia (Rosen et al., 1991). In vertebrates, moreover, where
the act of deglutition
is clearly distinguishable
from other feeding-related behaviors (Miller, 1982), bouts of swallowing
activity can be triggered by the stimulation
of discrete sensory fiber
tracts running in the superior laryngeal nerve (Jean and Car,
1979). In all these cases, the triggering pathways are assumed
to impinge upon discrete neuronal networks that are each dedicated to a particular aspect of overall feeding behavior. This is
fundamentally
different from the example reported here in that
the neurons that appear to satisfy swallowing in lobsters are also
involved in other food processing tasks when swallowing
is not
being expressed (see below).
Construction of a pattern-generating network with neurons
belongingto d$erent networks
The crustacean STNS has been considered to embody four discrete and essentially independent
pattern-generating
networks
on the basis of their different neuronal composition,
activity
patterns, and the muscle assemblages they control (Selverston
and Moulins,
1987). An important
feature of the STNS is that
unlike many other systems, motor neurons are themselves in-
642
Meyrand
et al. - Functional
Reconfiguration
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Neural
Networks
A
PS
silent
Oes.
C
B
Post
PS active
Swallowing
Net.
PS
activity
Oes.
Net.
Net.
I
I
Gastric
Net.
Pyloric
Gastro-pyloric
Net.
Net.
0
Oes
Oes
Gast
Gast
PYl
PS
PYl
PS
n
m
m
m
0
N
Figure 12. Diagrammatic representation of the functional construction of the swallowing network by PS neurons from elements belonging to
different STNS networks. A, When PS is silent, the esophageal, gastric, and pyloric networks (top) generate independent rhythmic output patterns
(middle) involved in regionally specific and separate behavioral tasks (bottom). B, When PS is rhythmically active, it drives opening of the OCS
valve (bottom), and by breaking down preexisting STNS networks and using certain neurons, it constructs a single novel network (top) that generates
a coordinated motor pattern (middle) appropriate for swallowing behavior. C, When PS is again silent, the OSC valve closes (bottom) and motor
units rostra1 to the OCS valve (i.e., esophageal elements) immediately resume their original network activity while units (i.e., gastric and pyloric)
controlling regions more caudal to the sphincter continue to generate a single pattern before resuming their separate activities.
tegral membersofthese central circuits. Thus, the output pattern
of an identified motor neuron provides an accurate indication
both of the behavior for which it is responsibleand the central
activity that determinesthis output. To date the capacity of the
STNS to generateswallowing-like behavior, in addition to the
four regional motor tasksof the foregut, hasnot beendescribed.
This is perhapsnot surprisingsincethe underlying circuits preferentially and spontaneouslyexpresstheir separateregion-specific patterns in vitro. Thus, given the rarity with which the PS
neurons are themselvesspontaneouslyactive in isolated preparations, evidence that under certain circumstancesthesenetworks can be reconstituted into an entirely different functional
network has failed to arise.
While a detailed analysisof the mechanismsinvolved in this
dynamic reconfiguration of multiple STNS output by PSis outside the scope of the present report (Simmers et al., 1991; J.
Simmers, P. Meyrand, and M. Moulins, unpublished observations), several major featuresare noteworthy here. First, PS is
able to dismantle preexisting target circuits becauseit can alter,
in a long-lasting fashion, the expressionof intrinsic properties
of many individual STNS neurons. For example, a previous
study (Cazalets et al., 1990b; seeFig. 8) has shown that for
certain neurons, such as the lateral pyloric neuron LP, the intemeuron is able to inhibit their inherent plateauing properties
in a manner that far outlasts (by several tens of seconds)the
dischargeof PS itself. The fact that LP switches from a plateauing to a “nonplateau” state has profound consequences
for
the functional integrity of the pyloric network asa whole. When
LP is no longer in a bistable state, (1) it is unable to respondto
phasic inputs from the other neurons within its own network
and the cell remainssilent, and (2) thesepyloric partners,which
are normally strongly influenced by synaptic input from LP, are
now free to have their activity shapedby direct input from PS.
For other stomatogastricneurons, PS enhancesor activates intrinsic burst-generatingproperties (Cazaletset al., 1990b; Simmers et al., 199I), again leading to PS-timed modifications in
output of the networks to which thesecells belong. Second,via
fast conventional postsynaptic actions(excitatory or inhibitory)
that it exerts on a further subpopulation of stomatogastricneurons (seeFig. 2&p, Cazalets et al., 1990a,b; Meyrand et al.,
The Journal
199 1; Simmers et al., 199 l), PS is able to drive these diverse
elements in phase (e.g., VD in Figs. 6, 8) or out of phase (e.g.,
LG in Fig. 6) with its own activity pattern. Third, the rhythmic
activity of the swallowing pattern is generated by the PS neurons
themselves (Fig. 7). These neurons appear to be endogenous
bursters, expressing properties that characterize endogenous oscillators in general (Pinsker, 1977; Meyrand and Moulins, 1986).
(1) The PS neurons can oscillate and produce bursts without
evident synaptic potentials or after isolation from regions of
possible synaptic input (data not shown), (2) they become rhythmically active in a voltage-dependent manner in response to
direct tonic depolarization (Fig. 4B), and (3) the phase of the
rhythm cycle can be reset by brief experimental perturbations
(Fig. 4C). Thus, the ability of PS to reconfigure already operating
STNS networks into a single new functional network appears
to reside in the diversity of its synaptic influences acting in
combination with the cell’s own intrinsic membrane properties.
Comparative aspects of network reconfiguration
In a wider context, our data begin to challenge the concept of
neuronal circuits as discrete predefined assemblages within the
CNS, since they show that a network required for a complete
behavioral task can be built up entirely from a pool of neurons
already participating in other different behaviors. In other words
a functional network can be seen as a strictly labile entity that
according to modulatory influences may exist only to satisfy the
demands of a particular behavioral situation.
Although it is now well established from invertebrates (Getting, 1989; Satterlie, 1989; Harris-Warrick
and Marder, 199 1)
and vertebrates (Grillner et al., 1991) alike that a single anatomically defined network can produce different forms of the
same behavior due to modulatory instruction, it has only recently emerged that the actual composition of a network is a
plastic phenomenon with neurons being able to participate in
more than one circuit and hence more than one behavior. To
date the cellular basis of such network plasticity has been most
extensively revealed in the crustacean STNS. In spiny lobsters,
for example, a single neuron can switch from one pattern generator to another in response either to the activation of a sensory
input pathway (Hooper and Moulins, 1989) or to exogenous
peptidergic stimulation (Dickinson and Marder, 1989). In the
crab Cancer borealis, neurons ofboth the pyloric or gastric CPGs
can fire in time with either network (Weimann et al., 1991)
while in Pam&us interruptus, bath application of the neuropeptide red pigment-concentrating
hormone (RPCH) can fuse
two independent rhythmic networks to form a novel conjoint
rhythm (Dickinson et al., 1990). In these cases the cellular mechanisms underlying such alterations in network integrity appear
to be the same as for modulation within a single network, that
is, via alterations in the intrinsic firing properties of component
neurons (Hooper and Moulins, 1989) or changes in strength of
synaptic connections between networks that otherwise function
independently (Dickinson et al., 1990). Our results add a significant new dimension to this theme in that rather than a switch
of individual neurons between different ongoing rhythms or a
functional merger of whole active circuits, we find that via their
endogenous properties and multiaction postsynaptic effects (Cazalets et al., 1990b; Simmers et al., 1991; Simmers, Meyrand,
and Moulins, unpublished observations), a single pair of interneurons can selectively dismantle several independently operating networks and construct a new network that bears no structural
or functional resemblance to the circuits of origin (see Fig. 12).
of Neuroscience,
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This dynamic construction of a neural network also differs
fundamentally from the “polymorphism”
(Getting, 1989) seen
in other motor pattern-generating systems. In the sea slug Tritonia, for example, the same intemeuronal network that generates escape swimming (Getting, 198 1, 1983) is also involved
in reflex withdrawals under certain conditions (Getting and Dekin, 1985). However, here the switch from one behavior to the
other does not require the dissolution of one network to create
another, but rather, relies on the functional assimilation of different subsets of neurons into the same basic circuit. In the
pteropod mollusk Clione limacina, the central network for
swimming can be rewired to produce two distinct motor patterns
underlying “weak” and “intense” locomotor behavior (Arshavsky et al., 1985a,b, Satterlie, 1989). Here again, the reconfiguration of the swim network is due to the active participation of
an identified interneuron that remains silent during “weak”
swimming (Arshavsky et al., 1985b). Thus, in both these systems
and unlike the situation reported here, the switch from one
functional network to another depends on the simple annexation
of different elements to a parent circuit that otherwise maintains
its structural and operational integrity.
In vertebrates, apparently straightforward
behaviors such as
walking and swimming may involve hundreds of different muscles that must be coordinated to produce meaningful behavior.
In the lamprey, for example, undulatory swimming movements
are coordinated by a chain of segmental pattern-generating networks (Grillner et al., 199 1) that can reverse their phase coupling
to produce spinal output appropriate for either forward or backward locomotion (Grillner and Matsushima, 199 1). In cats,
moreover, certain respiratory neurons can be involved in the
control of vomiting (Miller et al., 1987, 1990) coughing and
sneezing (Jakus et al., 1985). Here again, although these cases
illustrate that entire unit networks or subsets of these circuits
can be recombined to produce different motor acts, they still
fall short of the restructuring capability described in the present
report, namely, that according to a particular behavioral requirement, the nervous system is able dynamically to specify a
completely new functional network from individual neurons of
disparate origin.
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