Lesion in the lateral cerebellum specifically produces overshooting of the toe trajectory in leading forelimb during obstacle avoidance in the rat.

During locomotion, stepping over an obstacle under visual guidance is crucial to continuous safe walking. Studies of the role of the central nervous system in stepping movements have focused on cerebral cortical areas such as the primary motor cortex and posterior parietal cortex. There is speculation that the lateral cerebellum, which has strong anatomical connections with the cerebral cortex, also plays a key role in stepping movements over an obstacle, although this function of the lateral cerebellum has not yet been elucidated. Here we investigated the role of the lateral cerebellum during obstacle avoidance locomotion in rats with a lateral cerebellar lesion. A unilateral lesion in the lateral cerebellum did not affect limb movements during overground locomotion. Importantly, however, the lesioned animals showed overshooting of the toe trajectory specific to the leading forelimb ipsilateral to the lesion when stepping over an obstacle, and the peak toe position, in which the toe is maximally raised during stepping, shifted away from the upper edge of the obstacle. Recordings of EMG activity from elbow flexor and extensor muscles suggested that the overshooting toe trajectory in the ipsilateral leading forelimb possibly resulted from sustained elbow flexion and delayed elbow extension following prolonged activity of the biceps brachii. These results suggest that the lateral cerebellum specifically contributes to generating appropriate toe trajectories in the ipsilateral leading forelimb and to controlling related muscle activities in stepping over an obstacle, especially when accurate control of the distal extremity is achieved under visual guidance.

[1]  F. Sultan,et al.  Functional localization in the cerebellum , 2011, Cortex.

[2]  W T Thach,et al.  The cerebellum and the adaptive coordination of movement. , 1992, Annual review of neuroscience.

[3]  T. Drew,et al.  Motor cortical cell discharge during voluntary gait modification , 1988, Brain Research.

[4]  Brook Galna,et al.  Obstacle crossing in people with Parkinson's disease: foot clearance and spatiotemporal deficits. , 2010, Human movement science.

[5]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[6]  D. Marple-Horvat,et al.  Neuronal activity in the lateral cerebellum of the cat related to visual stimuli at rest, visually guided step modification, and saccadic eye movements , 1998, The Journal of physiology.

[7]  J. F. Stein,et al.  Role of the cerebellum in the visual guidance of movement , 1986, Nature.

[8]  T. Drew Motor cortical activity during voluntary gait modifications in the cat. I. Cells related to the forelimbs. , 1993, Journal of neurophysiology.

[9]  Jan Voogd,et al.  CHAPTER 9 – Cerebellum , 2004 .

[10]  Mario Manto,et al.  Journal of Neuroengineering and Rehabilitation Mechanisms of Human Cerebellar Dysmetria: Experimental Evidence and Current Conceptual Bases , 2022 .

[11]  Richard Apps,et al.  Behavioural Significance of Cerebellar Modules , 2010, The Cerebellum.

[12]  M. Sirota,et al.  Integration of motor and visual information in the parietal area 5 during locomotion. , 2003, Journal of neurophysiology.

[13]  J. Hore,et al.  Movement and electromyographic disorders associated with cerebellar dysmetria. , 1986, Journal of neurophysiology.

[14]  N. Ramnani The primate cortico-cerebellar system: anatomy and function , 2006, Nature Reviews Neuroscience.

[15]  Xiaofeng Lu,et al.  Topographic distribution of output neurons in cerebellar nuclei and cortex to somatotopic map of primary motor cortex , 2007, The European journal of neuroscience.

[16]  D. Marple-Horvat,et al.  The lateral cerebellum and visuomotor control. , 2005, Progress in brain research.

[17]  Dai Yanagihara,et al.  Characteristics of leading forelimb movements for obstacle avoidance during locomotion in rats , 2012, Neuroscience Research.

[18]  Kim Lajoie,et al.  Lesions of area 5 of the posterior parietal cortex in the cat produce errors in the accuracy of paw placement during visually guided locomotion. , 2007, Journal of neurophysiology.

[19]  Richard Apps,et al.  An internal model of a moving visual target in the lateral cerebellum , 2009, The Journal of physiology.

[20]  S. M. Morton,et al.  Mechanisms of cerebellar gait ataxia , 2008, The Cerebellum.

[21]  M. Sirota,et al.  The role of the motor cortex in the control of vigour of locomotor movements in the cat. , 1993, The Journal of physiology.

[22]  D. Marple-Horvat,et al.  Rhythmic neuronal activity in the lateral cerebellum of the cat during visually guided stepping , 1999, The Journal of physiology.

[23]  J Massion,et al.  Spatial organization of the cerebello-thalamo-cortical pathway. , 1972, Brain research.

[24]  P. Strick,et al.  Cerebellum and nonmotor function. , 2009, Annual review of neuroscience.

[25]  G. Paxinos The Rat nervous system , 1985 .

[26]  Marco Molinari,et al.  Cerebellar input to the posterior parietal cortex in the rat , 2002, Brain Research Bulletin.

[27]  P. Strick,et al.  Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate , 2003, The Journal of Neuroscience.

[28]  Laura Petrosini,et al.  A century of cerebellar somatotopy: a debated representation , 2004, Nature Reviews Neuroscience.

[29]  Amy J. Bastian,et al.  Cerebellar damage produces context-dependent deficits in control of leg dynamics during obstacle avoidance , 2004, Experimental Brain Research.

[30]  Pavel V Zelenin,et al.  Signals from the ventrolateral thalamus to the motor cortex during locomotion. , 2012, Journal of neurophysiology.

[31]  L. Christensen,et al.  University of Birmingham Disruption of state estimation in the human lateral cerebellum , 2007 .

[32]  H. Diener,et al.  Pathophysiology of cerebellar ataxia , 1992, Movement disorders : official journal of the Movement Disorder Society.

[33]  P. Strick,et al.  An unfolded map of the cerebellar dentate nucleus and its projections to the cerebral cortex. , 2003, Journal of neurophysiology.

[34]  Jun Tanji,et al.  Motor and non‐motor projections from the cerebellum to rostrocaudally distinct sectors of the dorsal premotor cortex in macaques , 2010, The European journal of neuroscience.

[35]  Kim Lajoie,et al.  Chapter 6--motor planning of locomotor adaptations on the basis of vision: the role of the posterior parietal cortex. , 2011, Progress in brain research.

[36]  T. Drew,et al.  Differential activity-dependent development of corticospinal control of movement and final limb position during visually guided locomotion. , 2007, Journal of neurophysiology.

[37]  Mitchell Glickstein How are visual areas of the brain connected to motor areas for the sensory guidance of movement? , 2000, Trends in Neurosciences.

[38]  Mario-Ubaldo Manto,et al.  A second mechanism of increase of cerebellar hypermetria in humans. , 2003, The Journal of physiology.

[39]  Dai Yanagihara,et al.  Gait modification during approach phase when stepping over an obstacle in rats , 2012, Neuroscience Research.

[40]  Trevor Drew,et al.  Discharge characteristics of neurons in the red nucleus during voluntary gait modifications: a comparison with the motor cortex. , 2002, Journal of neurophysiology.

[41]  Masao Udo,et al.  Hyperflexion and changes in interlimb coordination of locomotion induced by cooling of the cerebellar intermediate cortex in normal cats , 1979, Brain Research.

[42]  Thierry Pozzo,et al.  Kinematics of obstacle clearance in the rat , 2011, Behavioural Brain Research.

[43]  K. Sasaki,et al.  Electrophysiological studies of the projections from the parietal association area to the cerebellar cortex , 1975, Experimental Brain Research.

[44]  M. Sirota,et al.  The role of the motor cortex in the control of accuracy of locomotor movements in the cat. , 1993, The Journal of physiology.

[45]  J. Hore,et al.  Evidence that a disordered servo-like mechanism contributes to tremor in movements during cerebellar dysfunction. , 1986, Journal of neurophysiology.

[46]  Y. Shinoda,et al.  Cerebellar and cerebral inputs to corticocortical and corticofugal neurons in areas 5 and 7 in the cat. , 1995, Journal of neurophysiology.

[47]  M. Udo,et al.  Cerebellar control of locomotion: effects of cooling cerebellar intermediate cortex in high decerebrate and awake walking cats. , 1980, Journal of neurophysiology.

[48]  K. Pearson,et al.  Long-Lasting Working Memories of Obstacles Established by Foreleg Stepping in Walking Cats Require Area 5 of the Posterior Parietal Cortex , 2009, The Journal of Neuroscience.

[49]  T. Ruigrok,et al.  Organization of Cerebral Projections to Identified Cerebellar Zones in the Posterior Cerebellum of the Rat , 2012, The Journal of Neuroscience.

[50]  Kim Lajoie,et al.  A contribution of area 5 of the posterior parietal cortex to the planning of visually guided locomotion: limb-specific and limb-independent effects. , 2010, Journal of neurophysiology.

[51]  Kim Lajoie,et al.  Cortical mechanisms involved in visuomotor coordination during precision walking , 2008, Brain Research Reviews.

[52]  David A McVea,et al.  Object avoidance during locomotion. , 2009, Advances in experimental medicine and biology.

[53]  J. Hore,et al.  Cerebellar dysmetria at the elbow, wrist, and fingers. , 1991, Journal of neurophysiology.