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Functional Neuroanatomy for Posture and Gait Control

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Functional Neuroanatomy for Posture and Gait Control REVIEW ARTICLE https://doi.org/10.14802/jmd.16062 / J Mov Disord 2017;10(1):1-17 pISSN 2005-940X / eISSN 2093-4939 Functional ABSTRACT Here we argue functional neuroanatomy for pos- ture-gait control. Multi-sensory information such as Neuroanatomy somatosensory, visual and vestibular sensation act on various areas of the brain so that adaptable pos- ture-gait control can be achieved. Automatic process for Posture and of gait, which is steady-state stepping movements associating with postural reflexes including head- eye coordination accompanied by appropriate align- Gait Control ment of body segments and optimal level of pos- tural muscle tone, is mediated by the descending pathways from the brainstem to the spinal cord. Par- ticularly, reticulospinal pathways arising from the lat- Kaoru Takakusaki eral part of the mesopontine tegmentum and spinal locomotor network contribute to this process. On The Research Center for Brain Function and Medical Engineering, the other hand, walking in unfamiliar circumstance Asahikawa Medical University, Asahikawa, Japan requires cognitive process of postural control, which depends on knowledges of self-body, such as body schema and body motion in space. The cognitive in- formation is produced at the temporoparietal asso- ciation cortex, and is fundamental to sustention of vertical posture and construction of motor programs. The programs in the motor cortical areas run to ex- ecute anticipatory postural adjustment that is opti- mal for achievement of goal-directed movements. The basal ganglia and cerebellum may affect both the automatic and cognitive processes of posture- gait control through reciprocal connections with the brainstem and cerebral cortex, respectively. Conse- quently, impairments in cognitive function by dam- ages in the cerebral cortex, basal ganglia and cere- bellum may disturb posture-gait control, resulting in falling. Key Words Multisensory information; midbrain locomotor region; reticulospinal system; body schema; motor programs; Parkinson’s disease. Received: December 13, 2016 Accepted: December 15, 2016 Corresponding author: Kaoru Takakusaki, MD, PhD, The Research Center for Brain Function and Medical Engineering, Asahikawa Medical University, 2-1, 1-1 Midorigaoka- Higashi, Asahikawa 078-8511, Japan Tel: +81-166-68-2884 Fax: +81-166-68-2887 E-mail: [email protected] cc This is an Open Access article distributed under the terms of the Creative Commons Attri- bution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which per- mits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Copyright © 2017 The Korean Movement Disorder Society 1 JMD J Mov Disord 2017;10(1):1-17 GENERAL SCHEMA OF emotional, goal-directed behaviors are always ac- POSTURE-GAIT CONTROL companied by automatic process of postural control including balance adjustment and muscle tone regu- Figure 1 illustrates our recent understanding of lation. The subject is largely unaware of this process basic signal flows involved in motor control. Senso- which is evoked by sequential activations of neurons ry signals arising from external stimuli and/or inter- in the brainstem and spinal cord. Basic locomotor nal visceral information have various functions. For motor pattern is generated by spinal locomotor net- example, they are to be utilized for cognitive process- works that is termed as the central pattern generators ing such as production of working memory which (CPG). However, in order to learn motor skills or guides future behavior. Alternatively, they may affect behave in unfamiliar circumstance, the subject re- emotional and arousal states. Sensory signals are fur- quires cognitive posture-gait control that depends on ther available to detect and correct postural instabili- cognition of self-body information together with ty by acting on the cerebral cortex, cerebellum, and spatial localization of objects in extra-personal space. brainstem. Accordingly, animal initiates movements The cerebellum regulates the cognitive and auto- depending on either a “cognitive reference” or an matic processes of posture-gait control by acting on “emotional reference”.1,2 the cerebral cortex via the thalamocortical projection Voluntary movements are derived from intention- and on the brainstem, respectively. Both the feed- ally-elicited motor commands arising from the cere- forward information from the cerebral cortex via the bral cortex to the brainstem and spinal cord. On the cortico-ponto-cerebellar pathway and real-time sen- other hand, emotional reference may contribute to sory feedback via the spinocerebellar tract to the cer- emotional motor behavior which is generated by the ebellum may play major roles in these operations. projections from the limbic-hypothalamus to the The basal ganglia may also contribute to the modu- brainstem, such as fight or flight reactions.1,3,4 Re- lation of each process though its gamma-aminobu- gardless of whether the initiation is volitional or tyric acid (GABA)-ergic projections to the cerebral cortex and brainstem.2,5,6 The degree of GABAergic influence from the basal ganglia is regulated by the midbrain dopaminergic neurons.7 BRAINSTEM AND SPINAL CORD; CORE-STRUCTURES OF POSTURE-GAIT CONTROL In the absence of their forebrain, like a decere- brate cat, it can walk, trot and gallop. When the de- cerebration is made at precollicular-postmammilla- ry level, the cat initiates locomotion by electrical or chemical stimulation applied to the mesencephalic or midbrain locomotor region (MLR).1,8,9 However, if the neuraxis is transected slightly higher at the precollicular-premammillary level, cats can sponta- Figure 1. Basic signal flow involved in postural control. Multisensory signals neously elicit locomotion with well-coordinated pos- from the visual, vestibular, auditory, somatosensory (proprioceptive), and viscer- tural control.10 Therefore, a critical region exists be- al receptors act on various sites in the central nervous system. These signals tween these decerebrate levels. This area is recognized may provide cognitive and emotional references to the cerebral cortex and limbic system, respectively, so that the subject may elicit either voluntary movements or as the subthalamic locomotor region (SLR), which emotional motor behavior depending on the context. In each case, automatic mostly corresponds to the lateral hypothalamic area. 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, Stimulation of the SLR evoked locomotion after a cognitive postural control is particularly important when the subject learns motor large lesion was made in the MLR area,11 indicating skills and behaves in unfamiliar circumstance. See text for detail explanation. Modified from Takakusaki. Mov Disord 2013;28:1483-1491, with permission of that the SLR has direct connections with the brain- Wiley.6 stem locomotor pathway beyond the MLR. Howev- 2 Posture-Gait Control Takakusaki K er, the walking in the decerebrate preparations is rats by Sherman et al.21 show non-cholinergic neu- machine-like and is neither goal-directed nor adap- rons just medial to the PPN have projections to the tive to the environment. Hence, the SLR connec- spinal cord, while the cholinergic neurons of the PPN tions to the MLR are likely important for normal do not. This area at the mesopontine junction may be control of posture and gait. the true MLR. The dorsal neurons of this MLR area So far three locomotor regions have been identi- (laterodorsal tegmental nucleus) with spinal projec- fied in animals: the MLR in the mesopontine teg- tions are active in locomotion, while the ventral neu- mentum, the SLR and the cerebellar locomotor region rons are active in standing and do not have spinal pro- (CLR) in the mid-part of the cerebellum.12 Human jections. imaging study demonstrated that the organization of these supraspinal locomotor centers was preserved Functional organization of the reticular during the transition to bipedal locomotion human.13 formation in the control of posture The clinical relevance of these centers has so far been It is generally agreed that the reticulospinal tract largely neglected. (RST) contributes to regulation of the level of mus- cle tone. There may exist functional organization in Role of the mesencephalic area in the control the pontomedullary reticular formation (PMRF) in of posture and locomotion relation to the control of postural muscle tone (Fig- The MLR appears to be present in all classes of ure 3).15 Direct recording of reticulospinal neurons vertebrates.14 It likely includes the cuneiform nucle- (RSNs) revealed that those located in the dorso-me- us (CNF) and the pedunculopontine tegmental nu- dial part of the PMRF are active during the period cleus (PPN), although the precise location of the lo- of muscle tone suppression or muscular atonia (Fig- comotor regulation still remains a matter of debate. ure 3Aa), and those in the ventromedial part are ac- The PPN is located in the ventrolateral part of the tive during reflex standing due to decerebrate rigidity caudal mesencephalic reticular formation, composed or hypertonus (Figure 3Ab). Accordingly, functional of a heterogeneous population of neurons, containing topographical organization may exist in the PMRF GABA and glutamate in addition to acetylcholine.15 in the control of postural muscle tone. On the other Different neuronal
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