Takakusaki 2016

Advanced Robotics
ISSN: 0169-1864 (Print) 1568-5535 (Online) Journal homepage: http://www.tandfonline.com/loi/tadr20
Neural substrates involved in the control of

posture
Kaoru Takakusaki, Mirai Takahashi, Kazuhiro Obara & Ryosuke Chiba
To cite this article: Kaoru Takakusaki, Mirai Takahashi, Kazuhiro Obara & Ryosuke Chiba (2017)
Neural substrates involved in the control of posture, Advanced Robotics, 31:1-2, 2-23, DOI:
10.1080/01691864.2016.1252690
To link to this article: http://dx.doi.org/10.1080/01691864.2016.1252690
Published online: 06 Dec 2016.
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Advanced Robotics, 2017
VOL. 31, NOS. 1–2, 2–23
http://dx.doi.org/10.1080/01691864.2016.1252690
SURVEY PAPER
Neural substrates involved in the control of posture

Kaoru Takakusaki, Mirai Takahashi, Kazuhiro Obara and Ryosuke Chiba
The Research Center for Brain Function and Medical Engineering, Asahikawa Medical University, Asahikawa, Japan
ABSTRACT ARTICLE HISTORY

This review argues neuronal mechanisms of postural control. Multi-sensory information such as Received 19 April 2016
somatosensory, visual, and vestibular sensation act on various areas of the brain so that adaptable Accepted 23 May 2016
postural control can be achieved. Automatic process of postural control, which is termed as KEYWORDS
postural reflexes including head–eye coordination accompanied by appropriate alignment of Body schema; postural
body segments, is mediated by the descending pathways from the brainstem. Cooperation of the verticality; postural
vestibulospinal, reticulospinal, and tectospinal tracts contributes to this process. On the other hand, reflex; motor programing;
walking in unfamiliar circumstance requires cognitive process of postural control, which depends anticipatory postural
on knowledge of self-body, such as body schema, sense of postural verticality, and body motion adjustment
in space. Such a bodily cognitive information is produced at the temporoparietal cortex. They are
fundamental to sustention of vertical posture and construction of motor programs. The programs
then run to execute anticipatory postural adjustment which is appropriate for achievement of goal-
directed movements. The basal ganglia and cerebellum may affect both the automatic and cognitive
processes of postural control through reciprocal connections with the brainstem and cerebral cortex,
respectively. Consequently, impairments in cognitive function in addition to damages in the motor
cortex, basal ganglia, and cerebellum may disturb appropriate postural control, resulting in falling.
Abbreviations: APA: anticipatory postural adjustment; BF: basal formation; CNF: cuneiform nucleus;
COR: cervicoocular reflex; CPGs: central pattern generators; CCR: cervicocollic reflex; DA: dopamine;
DBS: deep brain stimulation; E: extensor motoneuron; D: flexor motoneuron; FN: fastigial nuclei;
GABA: gamma aminobutyric acid; LC: locus coeruleus; LVST: lateral vestibulospinal tract; M1: primary
motor cortex; MLR: midbrain locomotor region; MVST: medial vestibulospinal tract; PD: Parkinson’s
disease; PIVC: parieto-insular vestibular cortex; PM: premotor area; PMRF: pontomedullary reticular
formation; PPN: pedunculopontine tegmental nucleus; PRF: pontine reticular formation; RD:
raphe dorsalis; RSNs: reticulospinal neurons; S1: primary sensory cortex; SC: superior colliculus;
SMA: supplementary motor area; SNc: substantia nigra pars compacta; SNr: substantia nigra pars
reticulate; VCR: vestibulocollic reflex; VOR: vestibuloocular reflex
1. Introduction process of postural control, which requires self-body

information together with spatial localization of object
Postural control is one of the innate motor functions in
in extra-personal space so that one can appropriately
animals. Particularly, the human being acquires the ability
adjust one’s posture in advance to achieve goal-directed
of standing and walking by legs and within 15 months
movements. Processing of the cognitive information by
after birth. During this developmental period, one has
the higher brain function is particularly important when
learned two aspects of postural control mechanisms: one
the subject has to learn motor skills and to behave in unfa-
is to build up upright body posture against the forces of
miliar circumstance.[1–3]
gravity, and the other is to obtain the knowledge of the
Intentional locomotor control, such as gait initia-
orientation and motion of the body in space. Here, we
tion and avoiding obstacles during walking, is skillful
define the former as the automatic process of postural
and goal-directed motor performance that requires the
control, because the subject is largely unaware the auto-
optimal response in a context involving external and
matic adjustment of postural muscle tone, maintenance
internal constraints. The external constraints are those
of upright standing, and the postural reflexes or postural
imposed by the environmental conditions under which
reactions that accompany purposeful action. On the other
the action is performed under such as the gravitational
hand, the latter mechanism is defined as the cognitive
CONTACT Kaoru Takakusaki kusaki@asahikawa-med.ac.jp

© 2016 Taylor & Francis and The Robotics Society of Japan
ADVANCED ROBOTICS 3
forces, the reaction forces from the supporting surfaces, This review consists of two purposes. One is to
imposed accelerations and obstacles. The internal con- describe overview of the basic framework of the neural
straints are those which originate from the body itself: mechanisms of posture control. Here, we first summa-
the geometrical configuration of the body segments, the rize the current understanding of the core systems of the
inertial characteristics of the segments, and the internal automatic process of postural control, which is mostly
forces associated with muscle contraction. Therefore, the achieved by the brainstem and spinal cord. Another pur-
central organization of a motor skill requires motor pro- pose is to consider how the forebrain structures and cer-
grams which take into account all the external and internal ebellum act on the brainstem–spinal cord systems so that
constraints. It requires long-term learning as the result cognitive process of postural control can be achieved. A
of which these constraints are predicted in the central particular emphasis is placed on the importance of the
control of the motor act.[4] The predictive operations of cortico–brainstem projection systems in the execution of
postural programs as well as those of precise movements the higher ordered cognitive process of postural control,
of particular body parts utilize the cerebral cortex, basal such as sustention of vertical posture and anticipatory
ganglia, cerebellum, and brainstem, whose influences are postural adjustment (APA) for full execution of goal-
brought to bear through the descending systems acting directed movements.
on the spinal cord.[4–6] The critical question is, there-
fore, how the central nervous system learns to organize
2. Basic framework of the motor control
motor skills by predicting and fulfilling the external and
internal constrains. Answering to this ultimate question in Figure 1 illustrates basic signal flows involved in motor
the motor control is of extreme value for neuroscientists control. Sensory signals arising from external stimuli and/
including clinicians and therapists so that they enable to or internal visceral information have various functions.
understand pathophysiological mechanisms and create For example, they are to be utilized for cognitive process-
innovative treatment strategies of posture–gait disorders. ing such as production of working memory which guides
These knowledges are also quite available for engineers to future behavior. Alternatively, they may affect emotional
artificially design bipedal posture–gait models. and arousal states. Sensory signals are further available
Figure 1. Basic signal flow involved in postural control.

Notes: Multisensory signals from the visual, vestibular, auditory, somatosensory, and visceral receptors act on various sites in the central nervous system. These
signals may provide cognitive and emotional references to the cerebral cortex and limbic system, respectively, so that the subject may elicit either voluntary
movements or emotional motor behavior depending on the context. In each case, automatic process of postural control, such regulation of postural muscle tone
and basic postural reflexes, by the brainstem and spinal cord is required. On the other hand, cognitive postural control is particularly important when the subject
learns motor skills and behaves in unfamiliar circumstance. See text for detail explanation.
4 K. TAKAKUSAKI ET AL.
to detect and correct postural instability by acting on the and the ventromedial brainstem pathways. The dorsolat-
cerebral cortex, cerebellum, and brainstem. eral systems, which are composed of the corticospinal and
Accordingly, animals initiate movements depending on rubrospinal pathways, are involved in the control of pre-
either a ‘cognitive reference’ or an ‘emotional reference.’[7,8] cise limb–hand movement by acting on lateral cell groups
Voluntary movements are derived from intentionally in the spinal cord which mainly innervate distal flexor
elicited motor commands arising from the cerebral cor- muscles. These two pathways descend in the contralat-
tex to the brainstem and spinal cord. On the other hand, eral dorsolateral funiculus of spinal cord. On the other
emotional reference may contribute to emotional motor hand, the ventromedial pathways are important in main-
behavior which is generated by the projections from the taining balance and in postural fixation, both of which
limbic-hypothalamus to the brainstem, such as fight or relay especially on proximal muscles. The ventromedial
flight reactions.[8,9] Regardless of whether the initiation is pathways are phylogenetically the oldest component of
volitional or emotional, goal-directed behaviors are always the descending motor systems and consist of three major
accompanied by automatic process of postural control such tracts: the vestibulospinal, reticulospinal, and tectospinal
as balance adjustment and regulation of postural muscle tracts. These pathways descend in the ipsilateral ventral
tone. The subject is largely unaware of this process which columns of the spinal cord and terminate predominantly
is evoked by sequential activations of neurons in the brain- on interneurons and long propriospinal neurons in the
stem and spinal cord. However, in order to learn motor ventromedial part of the intermediate region, thus influ-
skills or behave in unfamiliar circumstance, the subject encing motoneurons that innervate axial and proximal
requires cognitive process of postural control that depends muscles. They also terminate directly on some moto-
on cognition of self-body information together with spatial neurons particularly those of the medial cell groups that
localization of object in extra-personal. innervate axial muscles. The wide area of termination of
The cerebellum regulates the cognitive and automatic individual axons is important in distributing control of a
processes of postural control by acting on the cerebral cor- variety of functional-related motor nuclei. In the follow-
tex via the thalamocortical projection and on the brain- ings, role of the above descending tracts is described in
stem, respectively. Both the feed-forward information relation to the postural control.
from the cerebral cortex and real-time sensory feedback
via the spinocerebellar tract to the cerebellum may play 3.1.1. Vestibulospinal tract
major roles in these operations. The basal ganglia may also The vestibular system receives labyrinthine and utricle
contribute to the modulation of each process though its inputs, and contributes to the generation of conjugate
GABAergic projections to the cerebral cortex and brain- eye movements, spatial orientation, and postural control
stem.[7,10,11] The degree of GABAergic influence from with head stability depending on gravity-based reference
the basal ganglia is regulated by the midbrain dopamin- frames (Figure 2(A)). The vestibular nuclei (medial, lat-
ergic neurons.[10–12] eral, and inferior nuclei) also receive proprioception and
visual sensation. The vestibular nuclei receive signals from
the cerebellum.[16,17]
3. Mechanisms of automatic process of postural
The medial vestibulospinal tract (MVST) in the cat
control
originates from the medial and inferior vestibular nuclei
Quadruped animals, like cats, decerebrated at precolli- and projects as far as the mid-thoracic region via ipsilateral
cular-premammillary level can stand, maintain equilib- ventral funiculus.[18] The MVST terminates to only axial
rium, and generate postural corrections in response to motoneurons. There are bilateral monosynaptic inhibition
lateral tilt of the supporting platform.[13,14] Therefore, of neck motoneurons [19] and monosynaptic excitation
an essential part of the mechanisms responsible for basic of contralateral neck motoneurons.[20] This tract also has
postural reactions in quadrupeds is located below the excitatory and inhibitory connections with lower cervical
decerebration level, that is, in the brainstem, spinal cord, and thoracic motoneurons.[19–21] On the other hand, the
and cerebellum. This section summarizes the mechanisms lateral vestibulospinal tract (LVST) extends ipsilaterally
of automatic process of postural control in which descend- throughout the length of the spinal cord and branch off
ing pathways from the brainstem to the spinal cord and their collaterals within each segment,[22] indicating that
intraspinal neural circuitry play pivotal role. the LVST has the potential to influence muscles located
in different parts of the body.[23,24]
The paired otolith organs, the utricles placed approx-
3.1. Functional architecture of the brainstem
imately horizontally, and the saccules vertically, respond
descending tracts
to linear acceleration including gravity. Their influence
Lawrence and Kuypers [15] classified descending path- leads to control neck muscles via the MVST during ori-
ways to spinal cord into main two systems: the dorsolateral enting head–eye movements (vestibuloocular reflex, see
ADVANCED ROBOTICS 5
Figure 2. Major descending pathways in the medial system.

Notes: (A) Vestibulospinal systems. The medial vestibulospinal tract originates from the medial and inferior vestibular nuclei and projects to the cervical and
mid-thoracic region via ipsilateral ventral funiculus. The lateral vestibulospinal tract extends ipsilaterally throughout the length of the spinal cord. The vestibular
nuclei receive visual, vestibular and proprioceptive sensations so that the medial and lateral vestibulospinal tracts contribute to vestibuloocular reflex and balance
control, respectively. The vestibular nuclei also receive corticofugal inputs from the vestibular cortex. This cortico-vestibular projection may contribute to sustain
vertical posture. (B) Reticulospinal systems. Neurons in the pontomedullary reticular formation which descend through the ventral and ventrolateral funiculi
constitute medial and lateral reticulospinal tracts, respectively. Reticulospinal neurons project to whole spinal segments. Therefore, the reticulospinal system
simultaneously organizes the contraction of the neck, trunk, and limb muscles so that synergistic control of postural muscle tone of whole body and postural
figure can be achieved. Flux of sensory information into the reticular formation contributes to the above process. Cortico-reticular projection arising from motor
cortical area (area 6) may be critically involved in anticipatory postural adjustment. (C) Tectospinal tract. Neurons in the superior colliculus project to upper cervical
cord and give off collaterals to the pontine gaze center in the medial reticular formation. Tectospinal tract is involved in head–eye coordination in response to
visual, auditory, and proprioceptive sensation. Cortico-collicular projection from frontal eye field (area 8) contribute to this process. See text for further explanation.
Section 3.2.1.1). On the other hand, these influences excite via the thalamocortical networks.[30] Projections within
ipsilateral extensor motoneurons of the limbs and trunk the brainstem and those descending to the spinal cord
and inhibit reciprocal flexor motoneurons via the LVST contribute to innate motor functions such as eye move-
(vestibulospinal reflex, see Section 3.2.1.2). ments,[31–33] eye–head coordination,[34,35] oral–
pharyngolaryngeal movements,[36–38] and control of
3.1.2. Reticulospinal tract posture and locomotion.[39–48]
The reticular formation – the area of the medulla and Medial and lateral reticulospinal tract arises from
pons composed mainly of interneurons and their pro- the pontomedullary reticular formation (PMRF), and
cesses – can best be considered as a rostral extension descends through the ventral and ventrolateral funiculi,
of the spinal intermediate zone into the brainstem. The respectively.[49–53] A considerable number of reticulo-
reticular formation receives proprioceptive, visceral,[25] spinal neurons (RSNs) send axons through the neuraxis
visual,[26,27] vestibular,[25,28] and auditory [29] sensa- from the cervical to lumbosacral segments (Figure 2(B)),
tions. The reticular formation also receives inputs from the and branch off their collaterals to each segment.[51–53]
forebrain structures (the cerebral cortex, limbic system, Such specific morphological features are functionally
and basal ganglia) and cerebellum in addition to spinal advantageous in orchestrating synergistic contractions
cord.[7–11] Therefore, the reticular formation contributes of the neck, trunk, and limb musculature.
to fundamental vital activities in relation to the vigilance In the cat experiments, electrical stimulation applied to
state of animals via the ascending and descending projec- the PMRF induce early (~20 ms), middle- (20–30 ms) and
tions. Ascending projections modulate cortical activities late- (30–100 ms) latency responses.[54–56] Concerning
to the early latency responses, reticular stimuli pro- center) so that saccadic eye movements are generated.
duces monosynaptic excitation of the flexor and exten- The output from the SC also produces head turning that
sor motoneurons of the neck, trunk, and limbs as well associates eye movements via the tecto-reticulospinal and
as monosynaptic inhibition of neck motoneurons.[57,58] tectospinal systems.[67]
Reticulospinal tract also has disynaptic inhibitory connec-
tions with extensor and flexor motoneurons of forelimb 3.1.4. Other descending systems
and hindlimb muscles.[55,56] However, axial motoneu- Three additional brainstem nuclei in motor function con-
rons, especially those of the neck, are the principal targets tribute to the ventromedial system: the interstitial nucleus
of the reticulospinal tract.[57,58] Because most RSNs has of Cajal, the raphe nuclei (a serotonergic cell group),
a conduction velocity faster than 80 m/s, early latency and the locus coeruleus (a noradrenergic cell group).
responses such as the monosynaptic and disynaptic effects Monoaminergic descending pathways such as the coeru-
can be due to activation of fast-conducting RSNs.[59,60] lospinal and raphespinal tracts belong to the muscle tone
The fast-conducting RSNs may also be involved in the excitatory system. Because monoaminergic fibers widely
activation of central pattern generators (CPGs) in spi- arborize in the gray matter,[68] the background excitabil-
nal cord to elicit locomotion.[48,61] The middle-latency ity of spinal neurons is increased by these tracts so that
effects are mostly excitatory whose time course is similar the spinal locomotor networks sensitively respond to the
to those evoked by the activation of coerulospinal and supraspinal signals and sensory afferents.
raphespinal tracts, indicating the involvement of the mon-
oaminergic systems in the middle latency effects. On the
3.2. Mechanisms of postural reflexes (postural
other hand, late-latency effects are exclusively inhibitory,
reactions)
which can be mediated by slow-conducting axons with
a velocity of 20–30 m/s.[54,55] The sites from which the 3.2.1. Balance control
late-latency inhibition was evoked were widely distributed 3.2.1.1. Vestibular control of head–eye coordination.
to the dorsomedial part of the PMRF [55,56] and the lat- The bony labyrinths in the inner ear contain several fluid-
eral part of the mesopontine tegmentum including the filled membranous sensory end organs, which comprise
pedunculopontine tegmental nucleus (PPN).[48,62,63] three mutually perpendicular semi-circular canals
In chronic cat preparation, reticular stimulation induced (vertical anterior, vertical posterior, and horizontal or
prominent late-latency inhibitory effects on motoneurons lateral) and two mutually perpendicular otoliths (utricle
during rapid eye movement (REM) sleep. However, they and saccule). This arrangement permits the most efficient
were completely diminished during wakefulness,[64,65] signal detection in three-dimensional space. The three
indicating that the neuronal mechanisms of generating canals communicate with the otoliths. Because motion
late inhibitory effects are involved in the state-dependent detected by these vestibular organs is encoded in a head-
modulation of postural muscle tone. fixed frame of reference, a coordinate transformation is
thus required to encode body motion.[69]
3.1.3. Tectospinal tract All head movements generate vestibular signals. Most
The tectospinal tract originates in the tectum of the body movements generate head movements due to the
midbrain (superior colliculus [SC]), a structure that is inertial forces acting on the head atop the flexible neck.
important for the coordinated control of head and eye Descending signals from higher centers also influence the
movements directed toward visual targets (eye–head coor- control of head and body movements through expecta-
dination; Figure 2(C)). Specifically, the superficial layers of tion of the consequences of actions. Multi-sensory signals
the SC receive direct retinal input, and are primarily visual (vestibular, visual, auditory, and somatosensory) converge
sensory in nature. They project to the visual thalamus and at the vestibular nuclei, and the output of which reflects
pretectum, and influence visual perception. The deep lay- the combination of these inputs. Loss of anyone of these
ers of the SC receive information of somatosensory and pathways to this center changes the nature of the response
auditory sensations in addition to visual information via to destabilization.
the superficial layers.[66] The SC receive efferents from Vestibular and cervical reflexes stabilize the head and
the basal ganglia and cerebellum. Sensory, association, neck by exciting neck muscles in opposition to head
and motor areas of the cerebral cortex provide another and body movements.[70] Sugiuchi et al. [71] showed
major source of collicular input. For example, projections that single MVST neurons innervated a functional set
from the visual cortex terminate superficially, while those of multiple neck muscles, and thereby implemented a
from the frontal eye fields (Area 8) target the deeper lay- canal-dependent, head-movement synergy. Because the
ers. The deeper layers provide the major projection to the medial vestibulospinal tract and reticulospinal tract have
paramedian pontine reticular formation (pontine gaze similar innervation patterns for neck muscles, both tracts
ADVANCED ROBOTICS 7
Figure 3. Mechanisms of vestibular reflexes.

Notes: Visual, vestibular, and proprioceptive signals converging to the vestibular nuclei contribute to vestibular reflexes, such as vestibuloocular, vestibulocollic,
and vestibulospinal reflexes. It should be noted that the cerebellum receives these sensory signals and regulates vestibular reflexes by acting vestibular nuclei and
reticular formation including the pontine gaze center. Generally, vestibular reflexes are responsible for stabilization of body equilibrium in response to eye, head,
and body movements in space. See text for detail explanation.
may control the same functional sets of neck muscles as CCR work jointly to stabilize the head position. These
schematically illustrated in Figure 3. reflexes are particularly important in conjunction with eye
The vestibular-neck reflex, or vestibulocollic reflex movements (Figure 3). Visual inputs which converge to
(VCR) aligns the head with respect to the gravitational the vestibular nuclei contribute to the vestibular reflexes
vertical. For example, a patient leaning forward over a in conjunction with head–eye coordination (vestibulooc-
walker uses this reflex to lift her head as she ambulates ular reflex [VOR]). Vestibular signals together with visual
so that her gaze is stabilized and oriented to the vertical information are sent to the pontine gaze center so that
position in space. The cervicocollic reflex (CCR) aligns the binocular eye movements are adjusted during head move-
head with respect to the position of the body. The CCR ments (Figure 3). The vestibuloocular neurons project-
was initiated by the cervical proprioceptors via reticulo- ing to the upper cervical cord where neck motoneurons
spinal neurons acting on cervical motoneurons; its actions are located may also contribute to VCR.[73,74] Because
complemented those of the VCR during movement.[72] If compensatory rotations of the eyes are observed during
the body is stationary and the head moves, the VCR and active head movements in labyrinthine-deficient animals
[72] and in patients with absent vestibular function,[75] 3.2.2. Control of postural muscle tone
proprioception from neck muscles may also contributes 3.2.2.1. Functional organization of the brainstem in
to this process (cervicoocular reflex [COR]). It should the control of postural muscle tone. It is generally
be mentioned that head–eye coordination also recruits agreed that the reticulospinal system contributes to
the activation of both the tectospinal and reticulospinal regulation of the level of muscle tone. There may exist
systems (Figure 3). Both tracts contribute to the c ontrol functional organization in the PMRF in relation to the
of eye movements and accompanying neck muscle control of postural muscle tone (Figure 4).[48] This
contractions.[34,76] was examined in decerebrate cat preparation which
maintained reflex standing posture due to decerebrate
3.2.1.2. Vestibulospinal reflexes. Vestibular-bodily rigidity (Figure 4(A-a)). Microsimulation applied to
interactions produced by the vestibulospinal tract the particular areas of the PMRF resulted in general
are defined as vestibulospinal reflexes (Figure 3). For suppression of muscle tone (Figure 4(A-b)), general
example, an activation of each semi-circular canal augmentation of muscle tone (Figure 4(A-c)) and
results in reciprocal limb movements so that the body tegmental reflexes or asymmetrical postural figures
is pushed into a vertical position by extending the (Figure 4(A-d)). The tegmental reflex is characterized
opposite limb.[77] On the other hand, with the head by extension of the unilateral limb and flexion of the
position fixed relative to the body, an activation of contralateral limb. It was observed that the ventromedial
each canal compensates neck and eye movements away part of the PMRF and the dorsal part of the rostral pons
from the direction of stimulation.[78] Otolith signals including the locus coeruleus (LC) and raphe dorsalis
from utricles and saccules also leads limb flexion and (RD) contributed to the muscle tone augmentation (blue
extension patterns that restore the head to a stable areas in Figure 4(B)). However, dorsomedial part of the
vertical position in response to horizontal or vertical PMRF and dorsolateral part of the rostral pons including
accelerations in response to gravity [79,80] with or the PPN were involved in muscle tone suppression
without vision.[81–83] (red areas in Figure 4(B)). Neuroanatomical studies
Interaction of the reticulospinal tract with vestibulo- revealed that RSNs in the dorsomedial and ventromedial
spinal tract plays an important role in the vestibulospinal PMRF descend through ventral and lateral funiculi,
reflex. Because reticular formation receives input from indicating that the ventral and lateral reticulospinal
various sources that could influence the control of pos- tract are responsible for muscle tone suppression and
ture, including vestibular, somatosensory, cortical, and augmentation, respectively. Tegmental reflex was evoked
cerebellar signals (Figure 2(B)), the reticulospinal tracts from the area between the inhibitory and excitatory
receive inputs from the vestibular labyrinths via projec- areas and the lateral part of the PMRF where few RSNs
tions from the vestibular nuclei and cerebellum.[16,84] arise in the cat (green areas in Figure 4(B)).
These combined signals can initiate a series of inter-spinal
reflexes that act to align the body segments.[79,85] 3.2.2.2. Role of the mesopontine tegmentum in the
Therefore, converging vestibular and spinal inputs either control of postural muscle tone and locomotion. The
combine or cancel their effects so that one can attain a mesopontine tegmentum including the PPN has been
position of optimum stability and orientation in space. recognized as one of the critical areas involved in
[86] When both the LVST and MVST were damaged in posture–gait control.[48,90,91] The PPN is located in the
cats, the VCR was not abolished, presumably as a result ventrolateral part of the caudal mesencephalic reticular
of the activation of the reticulospinal tract.[87] With formation, composed of a heterogeneous population of
the similar architectonic organization of descending neurons, containing GABA and glutamate in addition
fibers within the spinal cord, both the vestibulospinal to acetylcholine. Different neuronal types within the
and reticulospinal tracts corporate with stabilization of PPN area have different functions with their own
posture. inter-connections to multiple parts of the brain. There
Then, what is the functional difference between these are connections to the cerebral cortex, basal ganglia
two descending tracts? Matsuyama and Drew [88,89] nuclei, limbic areas, thalamus, brainstem, spinal cord,
examined the role of the reticulospinal and the vestib- and cerebellum. This key location including multiple
ulospinal tract neurons in the cat during locomotion on segregate functions renders determining the precise
an inclined surface. Specifically, the vestibulospinal tract function of these regions quite complicated.
controls primarily the overall level of postural muscle The PPN can be regarded as a part of the midbrain loco-
tone, while the reticulospinal tract has an additional role motor region (MLR), a functionally defined area involved
in determining the relative level of different muscles, par- in controlling locomotion. The MLR appears to be present
ticularly when the pattern is asymmetric. in all classes of vertebrates.[92,93] It likely corresponds to
ADVANCED ROBOTICS 9
Figure 4. Reticulospinal control of posture in decerebrate cat preparation.

Notes: (A) Postural changes in decerebrate cats. Head is fixed by stereotaxic apparatus, and body is suspended by rubber belt. The cat maintains reflex standing
posture due to decerebrate rigidity which is manifested by tonic activation of antigravity muscles (a). Stimulation of the pontomedullary reticular formation (50 Hz,
20–50 μA, 5–10 s) induces bilateral suppression (b) and augmentation (c) of postural tone, which are characterized by the changes in hip position. Reticular stimuli
also evoke tegmental reflex or asymmetrical posture which is characterized by extension of fore and hindlimbs of one side and flexion of combined with flexion
of limbs of the other side (d). (B) Functional topography of the pontomedullary reticular formation with respect to the control of hindlimb muscle tone. Results
obtained from five animals are superimposed on representative coronal planes of the rostral pons, caudal pons, and medulla. Sites from which either suppression
(red), augmentation (blue), or tegmental reflexes (green) was elicited in more than three out of five animals are marked. Sites from which the stimulation-induced
postural changes in more than four animals are indicated by darker colored squares; conversely, light colored squares indicate that the postural changes were
induced in three animals. Please see text for further explanation. (C) Organization of muscle tone inhibitory system. Cholinergic neurons in the pedunculopontine
tegmental nucleus (PPN) sequentially activate pontine reticular neurons and medullary reticulospinal neurons. (D) Organization of muscle tone excitatory system
and locomotor pathway. In addition to excitatory reticulospinal tract from the medioventral medulla, monoaminergic pathways arising from noradrenergic (NA)
and serotonergic (5-HT) neurons contribute to muscle tone augmentation. Locomotor pathway arises from glutamatergic neurons in the MLR, which corresponds
to the cuneiform nucleus (CNF) and a vicinity in the PPN, and activate excitatory reticulospinal tract. Signals from the MLR also excite monoaminergic pathways so
that excitability of spinal locomotor network is elevated. See text for further explanation. Abbreviations, LC; locus coeruleus, DR; dorsal raphe, IC; inferior colliculus,
SCP; superior cerebellar peduncle, LL; lateral lemniscus, NRPo; nucleus reticularis pontis oralis, CS; centralis superior, MLF; medial longitudinal fasciculus, NRPc;
nucleus reticularis pontis caudalis, 5ST; trigeminal spinal tract, RM; raphe magnus, TB; trapezoid body, SO; superior olive, VM; medial vestibular nucleus, NRGc;
nucleus reticularis gigantocellularis, NRMc; nucleus reticularis magnocellularis, RPa; raphe pallidus, P; pyramidal tract, ACh; acetylcholine, Glu; glutamate, NA;
noradrenaline, 5-HT; 5-hydroxy-triptamine (serotonin).
the cuneiform nucleus (CNF) and a vicinity of the PPN, but also modulate the locomotor pattern, and do this by
although the precise location of the locomotor regulation effects at the pontine level.[11,48] A recent study using
still remains a matter of debate.[48,92,94,95] The PPN optogenetically dissection of locomotor function of the
is active in suppressing muscle tone via its cholinergic three neurochemically distinct cell types (cholinergic,
projections to the pontine reticular formation (PRF) glutamatergic, and GABAergic) within the MLR showed
(Figure 4(C)), while the CNF mostly elicits locomotion. that the glutamatergic subpopulation of neurons encodes
Microstimulation of the transition zone between the locomotor state and speed, and is necessary and sufficient
two areas (ventral CNF, dorsal PPN) induced a mixture for locomotion while cholinergic neurons did not.[95]
of locomotor rhythm with associated muscle tone sup- In the ‘locomotor pathway,’ signals from the MLR also
pression.[11,48] Moreover, injecting atropine sulfate into activate medullary RSNs, in turn commanding the spinal
the PRF blocked the PPN-induced atonia but facilitated locomotor network to generate the oscillatory pattern of
MLR-induced locomotion, indicating that cholinergic locomotion (Figure 5).[47,96,97] Signals from the MLR
PPN neurons not only control the level of muscle tone may also activate monoaminergic descending pathways
Figure 5. Spinal control of postural muscle tone.

Notes: Supraspinal command signals acting on α-motoneuron, γ-motoneuron, and Ib inhibitory interneuron play an important role in the spinal mechanisms of
regulating muscle tone. Excitability of α-motoneuron is regulated by counterbalance between length feedback from muscle spindle afferents and force feedback
from tendon organs, via Ib inhibitory interneurons. Note that the degree of length feedback is regulated by γ-motoneurons that regulate the excitability of muscle
spindles. See text for further explanation.
including the coerulospinal and raphespinal tracts, acting autogenic inhibition), and flexion reflexes are involved
as a muscle tone excitatory system (Figure 4(D)).[98,99] in the control of posture. Particularly, stretch reflex and
Muscle tone inhibitory system arising from choliner- non-reciprocal inhibition play major role in static control
gic PPN neurons is mediated by pontomedullary RSNs of posture. On the other hand, interneuronal networks
(Figure 4(C)), which in turn inhibits α- and γ-motoneu- involved in reciprocal inhibition and flexion reflexes
rons that innervate extensor and flexor muscles, in parallel including crossed-extension reflex and are critical to pro-
with interneurons mediating reciprocal (Ia) inhibition, duce postural figures with extension–flexion movements
non-reciprocal inhibition (Ib inhibition), recurrent inhibi- of left–right leg alternation during walking. Integration
tion, and flexion reflexes. Possibly these inhibitory effects of all spinal reflex networks therefore can be essential to
can be mediated by a group of inhibitory interneurons full execution of muscle tone regulation during move-
in the Rexed lamina VII.[100] Presynaptic inhibition of ment. While spinal reflex networks generate rhythm and
primary sensory afferents was also induced by this system. pattern of locomotor movements through the activation
[101,102] Accordingly, an activation of this system may of the CPG, they play crucial role in supporting body
inhibit whole neuronal constituents of spinal reflex loops during stance phase of locomotion as well. Because spi-
including the CPG, resulting in the suppression of rhythm nal preparations in quadruped animals do not express
generation and locomotor pattern in addition to the level postural reflex described above, neural networks within
of postural muscle tone. On the other hand, selective acti- the spinal cord alone does not enable to control postural
vation of medullary RSNs by optogenetic stimulation in equilibrium.[96,97] Integration of descending supraspi-
rats suppressed locomotor activity without reduction of nal signals and peripheral sensory afferents at the level
muscle tone (halting).[103] It is therefore possible that the of spinal cord is further necessary for full execution of
inhibitory reticulospinal system enables to control muscle postural control.
tone and locomotor rhythm independently.
3.3.1. Spinal regulation of muscle tone
Basically, the level of muscle tone depends on the excitabil-
3.3. Spinal mechanisms of controlling posture and
ity of α-motoneurons. Figure 5 illustrates our understand-
movements
ing of the spinal mechanisms of muscle tone control during
Spinal circuitry involved in the stretch reflex, reciprocal static state. The excitability of α-motoneurons is determined
Ia inhibition, non-reciprocal inhibition (Ib inhibition or by signals in the descending motor commands and those of
ADVANCED ROBOTICS 11
Figure 6. Central and peripheral inputs to spinal locomotor network.

Notes: Spinal interneurons largely are responsible for generation of locomotor rhythm and pattern. Signals from ‘rhythm generating’ interneurons are sent
to ‘pattern formation’ interneurons so that the template of temporal and spatial patterns of muscle contractions operating on different limb or leg joints can
be produced. The template signals are forwarded to motoneurons innervating extensor (E) and flexor (F) muscles. Activity of spinal interneurons as well as
motoneurons is modified by both peripheral sensory afferents and supraspinal motor centers (cerebral cortex and brainstem) via corticospinal tract, locomotor
pathway, and muscle tone control systems (raphespinal, coerulospinal, and reticulospinal tracts). Accordingly, postural muscle tone and locomotor rhythm can be
simultaneously regulated by supraspinal signals. See text for further explanation.
length and force feedback signals from peripheral sensory 3.3.2. Spinal control of muscle tone during
organs. The load that is produced by muscle contractions locomotion
excites muscle spindles and tendon organs. Particularly, the Once animals start locomotion, muscle tone must be reg-
stretch reflex in which impulses generated by the excitation ulated depending on locomotor cycles. Figure 6 shows the
of muscle spindles, via group Ia afferents, monosynapti- current understanding of the spinal locomotor networks.
cally excite homonymous and agonistic motoneurons, is [8,47,96,100,110] A particular group of spinal interneu-
the most effective to motoneuronal excitability. Generally, ronal networks that generates rhythmic activity in the
supraspinal command signals equally act on α- and γ-mo- absence of rhythmic inputs is termed CPG.[43,96] The
toneurons (α–γ linkage). Therefore, the degree of the length rhythmic interneuronal activity is sent to the second-
feedback, which is expressed by the discharge rate of Ia order interneurons in the intermediate region (lamina IV–
afferents from muscle spindles, depends on both the load VII of Rexed), which shape ‘locomotor patterns’ of each
operating on the muscles and excitability of γ-motoneu- limb’s movements.[46,111] The signals are then transmit-
rons. The α–γ linkage is revealed in the actions evoked from ted to the target motoneurons innervating ipsilateral limb
the corticospinal,[104,105] vestibulospinal [106,107], and muscles through their excitatory and inhibitory actions.
reticulospinal [56] tracts. Inhibitory interneurons mediat- [46,96] Interneurons mediating reciprocal inhibition (Ia
ing autogenic or non-reciprocal inhibition (Ib inhibitory interneurons), non-reciprocal inhibition (Ib interneu-
interneurons) convert force feedback to inhibit the excit- rons), and recurrent inhibition (Renshaw cells) are likely
ability of α-motoneurons. Inhibitory Ib interneurons are included in this group.[96] On the other hand, lamina
also excited by supraspinal signals arising from the corti- VIII interneurons projecting to the contralateral side con-
cospinal, rubrospinal, and reticulospinal [108,109] tracts tribute to the left–right alternations of limb movements.
also act on inhibitory Ib interneurons. Accordingly, the [108,112] The rhythm and pattern of locomotor move-
excitability of motoneurons is regulated by counteraction ments are transmitted back to the supraspinal structures
between length feedback (positive feedback) and force feed- via the spinothalamic, spinoreticular, and spinocerebellar
back (negative feedback). Supraspinal commands modulate tracts so that the supraspinal structures monitor all events
these mechanisms. in the spinal cord.[46]
Activity of the spinal locomotor networks is modu- 4.1. Cortical contribution of postural control
lated by sensory afferents in a phase-dependent manner.
4.1.1. Cortical control of vertical posture
[96,111,113,114] For example, proprioceptors in muscles
How does the brain access to an internal estimate of body
at the hip joint are primarily responsible for regulating the
motion and postural verticality? Postural vertical is sup-
stance phase. Preventing hip extension suppresses step-
ported by a sense of verticality which is synthesized by
ping, whereas rhythmically moving the hip can entrain
visual, somatosensory, and vestibular information.[120–
the locomotor rhythm.[113] Afferents from propriocep-
124] Among various sensations, the vestibular sensation
tors in extensor muscles regulate transition from stance
is superior to other sensations in terms of absoluteness of
to swing phase. It should be critically mentioned that
sensation because it always refers the gravity,[125] and the
signals in Ib afferents from tendon organ in ankle exten-
vestibular system provides the brain with sensory signals
sor muscles inhibit homonymous motoneurons in rest,
about three-dimensional head rotations and translations.
while they excite extensor motoneurons during stance
Vestibulothalamic projections are bilateral and mainly
phase.[96,113] The functional consequence of this ‘reflex
involve the posterior thalamus.[126–128] While there
reversal’ is that the swing phase is not initiated until the
was no primary vestibular cortex that obtains projections
extensor muscles are unloaded and the forces exerted
exclusively from vestibular afferents, there are multiple
by these muscles are low. The continuous regulation of
presentations of vestibular information in the cerebral
extensor muscle tone by proprioceptive feedback presum-
cortex (Figure 7(A)).[129] These areas are distributed
ably allows automatic adjustment of force and length in
to the frontal eye field, premotor area, somatosensory
extensor muscles in response to the changes in loading
cortex, ventral intraparietal cortex, medial superior tem-
of the leg. Skin afferents also exert a powerful influence
poral area, and parieto-insular vestibular cortex (PIVC).
on the CPG.[46,96,113] Skin receptors are important to
Among them, the PIVC has dense connections with other
detect obstacles and adjust stepping to avoid them such
vestibular-relating cortical areas and receive information
as the ‘stumble-corrective reaction,’[115] which must be
from other sensory modalities.[125–132] It is now consid-
produced to a large extent by spinal circuits. Importantly,
ered that the posterior thalamus and the PIVC are areas
the corrective flexion movements are produced only if the
of interest for the internal model of postural verticality.
paw is stimulated during the swing phase. An identical
[133–137] Because the PIVC has descending connec-
stimulus applied during stance phase elicits the opposite
tions to the contralateral vestibular nuclei,[128,138–140]
response, an excitation of extensor muscles that reinforces
it can be postulated that the vestibular cortical system has
the ongoing extensor activity. This is another example of
a direct influence on the vestibulospinal system so that
the reflex reversal. The reflex reversal phenomenon is
one can maintain upright standing posture based on the
critically involved in postural control during locomotion.
information of the internal model of postural verticality
However, its mechanisms have not been elucidated.
(Figure 7(C)).
Postural verticality is often disturbed in pathological
4. Higher order regulation of posture by the conditions such as ‘pusher syndrome’ after stroke and ‘Pisa
cerebral cortex, cerebellum, and basal ganglia syndrome’ in advanced Parkinson’s disease. Stroke patients
with pusher syndrome actively push away from the ipsile-
Knowledge of the orientation and motion of the body in
sional side and have a tendency to fall toward their paretic,
space is important for the control of body, limb, and neck
contralesional side (the left side for right-hemisphere
posture as well as motion perception and spatial localiza-
patients). They had lesions including the parietal insular
tion of objects in extra-personal space.[116–118] Such a
cortex or posterior thalamus.[133,136,137,141] This phe-
knowledge is provided by integration of vestibular, soma-
nomenon is more prominent when patients are upright
tosensory, and visual sensory signals which occurs at both
compared to when lying down. Now the pusher phenom-
the cerebral cortex and cerebellum (Figure 7(A)).[119]
enon can be arising from a conflict or mismatch between
The brainstem receives direct inputs from the cerebral
visual and postural vertical.[133,137,142] Possible mech-
cortex and cerebellum in addition to the basal ganglia
anisms of Pisa syndrome will be discussed in section 4.3.
(Figure 1). Therefore, postural control largely depends
on the cognitive information derived from the higher
centers together with postural control systems within 4.1.2. Cortical and subcortical mechanisms of APA
the brainstem and spinal cord. Because postural control Precise visuomotor coordination, which is occurred at
is seriously impaired by damages in the cerebral cortex, the cerebral cortex, plays critical roles in the execution of
cerebellum, and basal ganglia, we review how these higher precise arm–hand movements such as reaching and grasp-
motor centers contribute to the postural control by acting ing.[2,3] Similarly, when a walking subject encounters
on the brainstem structures. obstacles, each leg must be placed with a high degree of
Figure 7. Cognitive process of postural control.

Notes: (A) Construction of bodily information. Sensory signals flowing into the central nervous system converge to the brainstem, cerebellum, thalamus, and
cerebral cortex. At the level of cerebral cortex, signals from the visual cortex, vestibular cortex and primary sensory cortex (S1) is integrated and internal model
of self-body, such as body schema and verticality can be constructed at the temporoparietal cortex including the vestibular cortex and posteroparietal cortex.
The cerebellum may also contribute to this process. (B) Motor programming. The bodily information is then transmitted to the supplementary motor area (SMA)
and premotor area (PM) where the information can be utilized as materials to produce motor programs. The motor cortical areas closely cooperate with the
basal ganglia and cerebellum so that appropriate motor programs are constructed. Intentional signal from the prefrontal cortex (PFC) may trigger to run motor
programs. (C) Postural control by corticofugal projections to the brainstem and spinal cord. The bodily information generated at the vestibular cortex may be
utilized for sustention of vertical posture via cortico-vestibular and vestibulospinal tract. The motor programs in the SMA/PM may include those for purposeful
movements and associating postural control. The postural control program may be utilized to generate anticipatory postural adjustment via cortico-reticular and
reticulospinal tract. Then motor programs are sent to primary motor cortex (M1) so that goal-directed purposeful movements can be achieved.
accuracy through the visuo–parieto–frontal cortical pro- pathways contribute to the APA by using animal experi-
jection, as in the subject has to modify the leg trajectory mentation and clinical examination. On the other hand,
in each step in order to achieve appropriate foot place- the PM/SMA may forward programs of precise leg–foot
ment.[143] Such a visuomotor coordination is particularly movement to the M1,[151] which, in turn, sends motor
necessary in quadrupeds because an obstacle is no longer command via the corticospinal tract. Consequently, cog-
within the visual field by the time the hindlimbs are step- nitive information processing in the temporoparietal
ping over it. Drew and his colleagues demonstrated, when cortex is essential for accurate gait control particularly
the posterior parietal cortex was bilaterally removed, the when the subject encounters an unfamiliar environment.
cat’s hindlimbs did not step over the obstacles if their fore- Therefore, the deficiency in the information processing
limbs cleared them.[144] They suggest that the posterior from the temporoparietal cortex to the frontal cortex may
parietal cortex must be engaged to register and store the cause errors in APA and gait difficulties such as the ‘freez-
temporospatial relationship between the obstacle and ing of gait.’ It follows that deficits in cognitive function in
one’s bodily information, such as body schema, in short- elder persons and in patients with Alzheimer’s disease are
term memory that is utilized to produce motor programs at higher risk of falling particularly when more cognitive
in the motor cortices so that the cat can precisely modify tasks are required.[152,153]
the limb trajectory based on visual information.[144–146]
To successfully achieve such an accurate control of limb
4.2. Cerebellar regulation of postural muscle tone
movements during walking, appropriate postural adjust-
ment that is optimized to the purposeful action has to Patients with damages in the medial cerebellum suffer
be preceded so that bodily equilibrium can maintained. from impaired postural control, often called as truncal
Therefore, the visuo–parieto–frontal cortical projection is ataxia, which is characterized by postural sway, hypo-
critically involved in the fulfillment of ongoing purposeful tonia, and discoordination of trunk–limb movements
control via anticipatory adjustments of posture.[4] It fol- (dis-synergia). The cerebellum has reciprocal connections
lows that both the intentional limb movements and APA with the brainstem, particularly the vestibular nuclei and
are programmed at motor cortical areas. reticular formation, cerebral cortex, and basal ganglia.
Then, what part of the motor cortex contributes to Through these connections, the cerebellum contributes
the programming of the APA? One of the most candi- to the control of postural reflexes, postural muscle tone,
date areas is the supplementary motor area (SMA) and and cognitive process of postural control.
premotor area (PM) (Figure 7(B)). Nakajima et al. [147]
demonstrated that inactivation of the leg area of the 4.2.1. Cerebellar modulation of the automatic
primary motor cortex (M1) by injections of muscimol process of postural control
(GABAA agonist) resulted in paresis of the contralateral Postural control by the cerebellum highly depends on
leg engaged in unrestrained bipedal walking in monkey. sensory afferents (Figure 7(A)). The labyrinthine signal
On the other hand, muscimol injections into the trunk/ ascends the VIII-th cranial nerve to the floccules and
leg regions of the bilateral SMA largely disturbed pos- vermis of the cerebellum in addition to the vestibular
tural control without inducing paralysis.[148] When an nuclei. Fastigial nuclei (FN), cerebellar nuclei located in
injection was administered into the dorsal PM, sponta- the medial part of the cerebellum, receive a copy of the
neous walking was maintained in the monkey; however, output of spinal cord in addition to peripheral sensory
the monkey could not start locomotion using sensory information via spinocerebellar tracts and the vermis.
cue. These findings indicate the presence of functional [154] The FN also receive visual [155] and vestibular
organization in the motor cortical areas in the control information.[156] These complex, multisensory features
of posture and locomotion in bipedal walking animals, may provide ‘an error-correction mechanism,’ which per-
and the SMA and PM may contribute to postural control mits FN neurons to affect motor functions such as coor-
during walking and initiation of gait, respectively. dinating postural responses during locomotion and other
It has been shown, while neurons in the M1 project movements which entail changes in limb position. The FN
mainly to the spinal cord, neurons in the SMA/PM have may therefore send highly integrated bodily information
dense projections to the PMRF in addition to the spinal during ongoing movements to the posture–gait-related
cord.[149,150] The reticulospinal tract innervates whole areas in the brainstem and motor cortical areas via the
spinal segments (Figure 2(B)) [112] so that it controls thalamocortical projections.[157]
postural muscle tone and symmetric postural figures.[48] Output from the FN to the brainstem contributes to the
Therefore, the corticoreticular and the reticulospinal tract control of postural muscle tone (Figure 7(C)). Electrical
may achieve postural preparation or APA (Figure 7(C)). stimulation applied to the mid-part of the cerebellar
It is particularly important to determine whether these white matter in decerebrate cats either increased [158] or
decrease the level of muscle tone.[159] The muscle tone ganglia in addition to the cerebral cortex may complement
augmentation is possibly caused by the activation of the the cerebellar role of cognitive process of postural control.
passing fibers arising from the bilateral FN. The cerebel-
lar stimulation possibly activated the excitatory reticu-
4.3. Basal ganglia control of posture with reference
lospinal tract and vestibulospinal tract so that extensor
to pathophysiology of Parkinson’s disease
muscle tone was bilaterally increased. On the other hand,
the decrease in the level of muscle tone is considered to Because posture–gait control is seriously impaired in PD,
be due to withdrawal of excitatory influence upon moto- which is the most famous basal ganglia disorder due to
neurons.[159] However, postural muscle tone is usually deficit in midbrain dopamine (DA) neurons, the basal
reduced in patients with mid-cerebellar lesions, cerebel- ganglia has long been functionally regarded to be predom-
lum generally contributes to maintain the level of muscle inantly involved in motor control but are increasingly rec-
tone. It can be considered that the FN possesses potential ognized to play an additional role in sensory processing,
capability to recruit and regulate postural- and locomo- cognition, and behavior.[171–173] Here, we particularly
tor-related subprograms which are distributed within the focus on the mechanisms of postural impairment in PD so
brainstem and spinal cord by the in-parallel activation of that understanding the contribution of the basal ganglia to
fastigio-spinal, fastigio-reticular, and fastigio-vestibular postural control is facilitated. Based on our understand-
pathways.[160–163] Therefore, the degree of α–γ linkage ing, postural disturbances in PD can be induced by follow-
which is provided by the vestibulospinal and excitatory ing mechanisms: (1) impairment of cognitive functions
reticulospinal tracts may be reduced in patients with due to failure of integrative sensory processing that may
cerebellar diseases, resulting in hypotonia. The hypotonia allow to construct internal postural model, (2) reduced
state may decrease the accuracy of the sensory feedback capability in motor programming due to reduced activity
and increase postural sway. in the motor cortical areas, and (3) reduced excitability
of muscle tone inhibitory system,[11,63] which induces
4.2.2. Cerebellar regulation of cognitive process of hypertonus (muscular rigidity) or co-contractions of
postural control extensor and flexor muscles of limb and trunk, resulting
Reciprocal connections between the cerebellum and cere- in flexion posture.
bral cortex (Figure 7(B)) may be critically involved in the
cognitive processes of postural control. It has been recently 4.3.1. Failure in dopaminergic and cholinergic
recognized that cerebellar output reaches vast areas of the systems in PD
neocortex including regions of the prefrontal and pos- Recent clinical studies suggest that the postural impair-
terior parietal cortices in addition to motor areas.[164] ments in PD is based on dysfunction of both the dopa-
The FN in the cerebellum, as well as the vestibular cortex minergic and non-dopaminergic, particularly cholinergic,
(PIVC), is critically involved in encoding internal postural system. Basically, damages of these chemo-specific sys-
model in space and self-motion.[119] Some studies have tems may critically contribute to posture–gait failure in
suggested the presence of FN projections to the parietal this disease. For example, a damage of DA neurons in
cortex,[165,166] motor cortex, and multimodal visual the substantia nigra pars compacta (SNc) which project
areas.[167] Reciprocal connection between the parietal to the basal ganglia nuclei may be considered to increase
cortex and the cerebellum may be involved in perception GABAergic inhibitory output from the basal ganglia.[174–
of body motion in space. Such a bodily information can 176] This may strongly inhibit the thalamocortical systems
be utilized to maintain upright posture during standing and brainstem structures (Figure 1). In addition, cholin-
and to achieve APA. The latter may involve reciprocal ergic neurons in the PPN (brainstem) and basal forebrain
connections between the motor cortical area (SMA/PM) (BF) are seriously damaged in PD.[177–180] Cholinergic
and cerebellum (motor loop) so that motor programs are PPN neurons project to the non-specific thalamocortical
constructed (Figure 7(C)).[6,32] Accordingly, cerebellar system,[181–183] basal ganglia nuclei including SNc-DA
disease patients may have problems in cognitive process neurons [184–186] and PMRF. On the other hand, cholin-
of postural control. However, the perception of verticality ergic BF projections to the cerebral cortex are necessary
in patients with cerebellar ataxia may only deteriorate in a for attentional performance and cognitive processing.
more advanced stage of the disease.[168] In addition, only [187] Therefore, disturbances in attention, sensorimotor
few abnormalities of APA were found in the cerebellar integration and cognitive processing in PD can be largely
disease patients compared to controls, while the patients attributed to the damage of the cholinergic systems that
appeared to be less able to use predictive information. have such unique anatomical and physiological position.
[169] Because the cerebellum is reciprocally connected Accordingly, both of the excessive inhibition from the
with the basal ganglia,[164,170] it is possible that basal basal ganglia and the damage of cholinergic systems may
impair cortical and subcortical (particularly the brain- and this process is seriously impaired in PD patients.
stem) functions. [203] Also, the dorsal part of the PM is involved in senso-
ry-guided gait control as suggested in bipedally walking
4.3.2. Failure in sensory processing and cognition in monkey.[147] Because the activity of dorsal part of the
PD PM was increased during visually-guided paradoxical
Cortical activity was substantially reduced in patients gait in PD patients, posture–gait programs in SMA/PM
in PD compared control subject during walking.[188] became reusable by the activation of visuo-motor path-
Reduced cortical activity may cause failure of integrative way.[204] Accordingly, failure in motor programming
sensory processing, which in turn, disturb construction in PD can be due to the decrease in excitability of the
internal postural model and motor programming. It has motor cortical areas in addition to the temporoparietal
been shown that a loss of cholinergic neurons in the BF cortices where cognitive self-bodily information can be
and PPN associates with fallers in PD.[177,189] Müller produced by integrating multi-sensory signals. Recently,
et al. [190] suggested that reduced activities in the cholin- role of the cerebellum in the pathophysiology of PD is
ergic PPN neurons may disturb multi-sensory integration highly recognized.[205,206] Because the cerebellum has
at the level of the thalamus. This may also explain why reciprocal connections with the basal ganglia in addition
patients in PD with more severe posture–gait instability to the cerebral cortex and brainstem, there is a need to
have a high risk of developing dementia.[191] Impairment elucidate whether the cerebellum participates in com-
of the central integration of sensory information, particu- pensatory mechanisms associated with the disease or
larly proprioception [192] or vestibular graviception,[193] contributes to the pathophysiology of PD.
may result in deficits of internal model of postural verti-
cality, which is possibly constructed at the temporopari- 4.3.4. Reduced activity in the posture–gait area in the
etal cortical area such as the vestibular cortex. Asymmetry midbrain
of the activity in the left and right vestibular cortex may Reduced excitability in the mesopontine tegmentum
induce leaning of upright standing posture, which is char- including the PPN/MLR can be also involved in
acterized as Pisa syndrome. Pisa syndrome is a dystonic posture–gait failure in this disease.[11,47,48] In decer-
lateroflexion of the trunk with a postural disturbance ebrate cats, the basal ganglia control locomotion and
resembling the leaning tower of Pisa, and is more often posture using different GABAergic output pathways of
observed in patients with advanced PD.[194] The marked the substantia nigra reticulata (SNr); the lateral part of
lateroflexion becomes worse during walking but is almost the SNr blocks the PPN-induced muscle tone suppres-
completely alleviated by passive mobilization or supine sion, whereas the medial part of the SNr suppresses
positioning.[195] Because PD without Pisa syndrome the MLR-induced locomotion.[11] Recent rat studies
also had deficiencies in postural verticality compared to confirm that inhibitory input from the SNc to the glu-
healthy controls,[192,196–198] mismatch between pro- tamatergic neurons in the MLR regulates locomotion.
prioception and vestibular gravitation may alter subjec- [95,205] In PD, GABAergic outputs of the basal gan-
tive postural vertical in PD, resulting in Pisa syndrome. glia are abnormally increased,[174–176] so excessive
Alternatively, asymmetry of basal ganglia output due to SNr-inhibition of the MLR may cause gait disturbance
cholinergic–dopaminergic imbalance in the striatum and muscle rigidity.[11] Muscle tone rigidity in PD is
[199,200] and disturbance of pallidal output [201,202] called as ‘lead-pipe like rigidity’ which is character-
may elicit imbalance of the thalamocortical processing ized by co-contraction of extensor and flexor muscles.
of vestibular information. Such a co-contraction is observed in neck, back, and leg
muscles, resulting in flexion posture including camp-
4.3.3. Failure in motor programming tocormia.[195]
The motor cortical areas including the M1, SMA and As one of clinical procedures for alleviating gait-
PM have connections with the basal ganglia and cerebel- posture deficiency in PD, deep brain stimulation (DBS)
lum, constituting motor loop that contributes to execu- targeting the PPN with the aim of stimulating remaining
tion and motor programming of voluntary movements cholinergic neurons.[207–210] The first studies using DBS
(Figure 7(B)).[6,32] Because of increasing inhibitory in advanced PD patients concluded that low-frequency
output from the basal ganglia to the thalamocortical stimulation of the PPN could be effective to control
projections in addition to reduced cognitive information freezing of gait and falls.[211,212] However, further

processing, the capability of producing motor programs clinical studies concluded that freezing of gait were mildly
in response to changes in circumstance can be deterio- improved by PPN–DBS but the overall results were rather
rated. In fact, the SMA contributes to APA for step initi- disappointing.[213–215] These results emphasize the need
ation via corticofugal projections to the PPN and PMRF, to determine the optimal surgical target.[215]
Disclosure statement [2] Murata A, Wen W, Asama H. The body and objects

represented in the ventral stream of the parieto-
No potential conflict of interest was reported by the authors. premotor network. Neurosci Res. 2016;104:4–15.
[3] Kravitz DJ, Saleem KS, Baker CI, et al. A new neural
framework for visuospatial processing. Nat Rev
Funding Neurosci. 2011;12:217–230.
This work was partially supported by grants from JSPS [4] Massion J. Movement, posture and equilibrium:
KAKENHI [grant number 26120004] and [grant number interaction and coordination. Prog Neurobiol.
25290001] for K.T., [grant number 26120006] and [grant num- 1992;38:35–56.
ber 15K06131] for R.C. KT is also supported by foundations [5] Brooks VB., III. Posture and locomotion. In: The neural
from the QOLER Medical Group and Sasson Hospital. basis of motor control. New York, NY: Oxford University
Press; 1986. p. 140–150.
[6] Middleton FA, Strick PL. Basal ganglia and cerebellar
Notes on contributors loops: motor and cognitive circuits. Brain Res Rev.
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ISSN: 0169-1864 (Print) 1568-5535 (Online) Journal homepage: http://www.tandfonline.com/loi/tadr20

Neural substrates involved in the control of

Kaoru Takakusaki, Mirai Takahashi, Kazuhiro Obara & Ryosuke Chiba

To link to this article: http://dx.doi.org/10.1080/01691864.2016.1252690

Published online: 06 Dec 2016.

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Download by: [FU Berlin] Date: 05 January 2017, At: 15:44

Neural substrates involved in the control of posture

ABSTRACT ARTICLE HISTORY

1. Introduction process of postural control, which requires self-body

CONTACT Kaoru Takakusaki kusaki@asahikawa-med.ac.jp

Figure 1. Basic signal flow involved in postural control.

Figure 2. Major descending pathways in the medial system.

Figure 3. Mechanisms of vestibular reflexes.

Figure 4. Reticulospinal control of posture in decerebrate cat preparation.

Figure 5. Spinal control of postural muscle tone.

Figure 6. Central and peripheral inputs to spinal locomotor network.

Figure 7. Cognitive process of postural control.

Disclosure statement [2] Murata A, Wen W, Asama H. The body and objects

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Disclosure statement [2] Murata A, Wen W, Asama H. The body and objects