Distinct neural circuits for control of movement vs. holding still.

In generating a point-to-point movement, the brain does more than produce the transient commands needed to move the body part; it also produces the sustained commands that are needed to hold the body part at its destination. In the oculomotor system, these functions are mapped onto two distinct circuits: a premotor circuit that specializes in generating the transient activity that displaces the eyes and a "neural integrator" that transforms that transient input into sustained activity that holds the eyes. Different parts of the cerebellum adaptively control the motor commands during these two phases: the oculomotor vermis participates in fine tuning the transient neural signals that move the eyes, monitoring the activity of the premotor circuit via efference copy, whereas the flocculus participates in controlling the sustained neural signals that hold the eyes, monitoring the activity of the neural integrator. Here, I review the oculomotor literature and then ask whether this separation of control between moving and holding is a design principle that may be shared with other modalities of movement. To answer this question, I consider neurophysiological and psychophysical data in various species during control of head movements, arm movements, and locomotion, focusing on the brain stem, motor cortex, and hippocampus, respectively. The review of the data raises the possibility that across modalities of motor control, circuits that are responsible for producing commands that change the sensory state of a body part are distinct from those that produce commands that maintain that sensory state.

[1]  H. Kornhuber,et al.  Natural and drug-induced variations of velocity and duration of human saccadic eye movements: Evidence for a control of the neural pulse generator by local feedback , 2004, Biological Cybernetics.

[2]  D. Robinson,et al.  Loss of the neural integrator of the oculomotor system from brain stem lesions in monkey. , 1987, Journal of neurophysiology.

[3]  Reza Shadmehr,et al.  TMS Perturbs Saccade Trajectories and Unmasks an Internal Feedback Controller for Saccades , 2011, The Journal of Neuroscience.

[4]  D. Munoz,et al.  Human eye-head gaze shifts in a distractor task. I. Truncated gaze shifts. , 1999, Journal of neurophysiology.

[5]  Uri Shalit,et al.  Descending systems translate transient cortical commands into a sustained muscle activation signal. , 2012, Cerebral cortex.

[6]  A. Opstal,et al.  Human eye-head coordination in two dimensions under different sensorimotor conditions , 1997, Experimental Brain Research.

[7]  Robert A McCrea,et al.  Nucleus prepositus. , 2006, Progress in brain research.

[8]  K. Cullen,et al.  Local Population Synchrony and the Encoding of Eye Position in the Primate Neural Integrator , 2015, The Journal of Neuroscience.

[9]  D. Robinson,et al.  The effect of cerebellectomy on the cat's bestibulo-ocular integrator. , 1974, Brain research.

[10]  S. Highstein,et al.  Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons. , 1986, The Journal of comparative neurology.

[11]  Stephan Riek,et al.  Feedforward compensation for novel dynamics depends on force field orientation but is similar for the left and right arms. , 2016, Journal of neurophysiology.

[12]  Mattias P. Karlsson,et al.  A hippocampal network for spatial coding during immobility and sleep , 2016, Nature.

[13]  P. Thier,et al.  Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease , 2007, The European journal of neuroscience.

[14]  Claude Ghez,et al.  Separate adaptive mechanisms for controlling trajectory and final position in reaching. , 2007, Journal of neurophysiology.

[15]  R. Sainburg,et al.  Differences in control of limb dynamics during dominant and nondominant arm reaching. , 2000, Journal of neurophysiology.

[16]  O. Hikosaka,et al.  Modulation of saccadic eye movements by predicted reward outcome , 2001, Experimental Brain Research.

[17]  D. Robinson,et al.  The oculomotor integrator: testing of a neural network model , 2006, Experimental Brain Research.

[18]  E. Bizzi,et al.  Eye-Head Coordination in Monkeys: Evidence for Centrally Patterned Organization , 1971, Science.

[19]  J. Kalaska,et al.  Motor cortex neural correlates of output kinematics and kinetics during isometric-force and arm-reaching tasks. , 2005, Journal of neurophysiology.

[20]  Hank Heijink,et al.  Different learned coordinate frames for planning trajectories and final positions in reaching. , 2007, Journal of neurophysiology.

[21]  Stephen C. Cannon,et al.  A proposed neural network for the integrator of the oculomotor system , 1983, Biological Cybernetics.

[22]  D. Zee,et al.  Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. , 1998, Journal of neurophysiology.

[23]  Andrzej Przybyla,et al.  Contralesional motor deficits after unilateral stroke reflect hemisphere-specific control mechanisms. , 2013, Brain : a journal of neurology.

[24]  Eliana M. Klier,et al.  Midbrain Control of Three-Dimensional Head Orientation , 2002, Science.

[25]  H. Noda,et al.  Effects of fastigial stimulation upon visually-directed saccades in macaque monkeys , 1991, Neuroscience Research.

[26]  Silvia Arber,et al.  Brainstem nucleus MdV mediates skilled forelimb motor tasks , 2014, Nature.

[27]  D. Zee,et al.  Spinocerebellar ataxia type 6: Gaze‐evoked and vertical nystagmus, Purkinje cell degeneration, and variable age of onset , 1997, Annals of neurology.

[28]  D. Zee,et al.  Oculomotor function in the rhesus monkey after deafferentation of the extraocular muscles , 2001, Experimental Brain Research.

[29]  F. A. Miles,et al.  Floccular lesions abolish adaptive control of post-saccadic ocular drift in primates , 2004, Experimental Brain Research.

[30]  T. Vilis,et al.  Generation of torsional and vertical eye position signals by the interstitial nucleus of Cajal , 1991, Science.

[31]  F A Miles,et al.  Visually induced adaptive changes in primate saccadic oculomotor control signals. , 1985, Journal of neurophysiology.

[32]  Helen J. Huang,et al.  A Representation of Effort in Decision-Making and Motor Control , 2016, Current Biology.

[33]  Lawrence Stark,et al.  Glissades—eye movements generated by mismatched components of the saccadic motoneuronal control signal , 1975 .

[34]  J. Kalaska,et al.  A comparison of movement direction-related versus load direction- related activity in primate motor cortex, using a two-dimensional reaching task , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  A. Fuchs,et al.  Fatigue resistance of human extraocular muscles. , 1983, Journal of neurophysiology.

[36]  D. Sparks,et al.  Spatial localization of saccade targets. I. Compensation for stimulation-induced perturbations in eye position. , 1983, Journal of neurophysiology.

[37]  P. Strick,et al.  Subdivisions of primary motor cortex based on cortico-motoneuronal cells , 2009, Proceedings of the National Academy of Sciences.

[38]  D. Robinson Oculomotor unit behavior in the monkey. , 1970, Journal of neurophysiology.

[39]  J. Kalaska,et al.  Differential relation of discharge in primary motor cortex and premotor cortex to movements versus actively maintained postures during a reaching task , 1996, Experimental Brain Research.

[40]  David L. Sparks,et al.  Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation , 2008, Experimental Brain Research.

[41]  D. Straumann,et al.  Gaze holding deficits discriminate early from late onset cerebellar degeneration , 2015, Journal of Neurology.

[42]  S. Scott,et al.  Random change in cortical load representation suggests distinct control of posture and movement , 2005, Nature Neuroscience.

[43]  B L McNaughton,et al.  Dynamics of the hippocampal ensemble code for space. , 1993, Science.

[44]  A. Georgopoulos,et al.  Static spatial effects in motor cortex and area 5: Quantitative relations in a two-dimensional space , 1984, Experimental Brain Research.

[45]  R. Shadmehr,et al.  Temporal Discounting of Reward and the Cost of Time in Motor Control , 2010, The Journal of Neuroscience.

[46]  D. Sparks,et al.  Corollary discharge provides accurate eye position information to the oculomotor system. , 1983, Science.

[47]  D. Sparks,et al.  Cerebellotectal pathways in the macaque: Implications for collicular generation of saccades , 1990, Neuroscience.

[48]  N J Gandhi,et al.  Endpoint accuracy in saccades interrupted by stimulation in the omnipause region in monkey , 1996, Visual Neuroscience.

[49]  Kaoru Yoshida,et al.  Premotor inhibitory neurons carry signals related to saccade adaptation in the monkey. , 2008, Journal of neurophysiology.

[50]  S. M. Highstein,et al.  Anatomy and physiology of intracellularly labelled omnipause neurons in the cat and squirrel monkey , 2004, Experimental Brain Research.

[51]  A. Fuchs,et al.  Characteristics and functional identification of saccadic inhibitory burst neurons in the alert monkey. , 1988, Journal of neurophysiology.

[52]  Neeraj J Gandhi,et al.  Effects of partial lidocaine inactivation of the paramedian pontine reticular formation on saccades of macaques. , 2003, Journal of neurophysiology.

[53]  K. Money,et al.  The vestibular system of the owl. , 1972, Comparative biochemistry and physiology. A, Comparative physiology.

[54]  C. Ghez,et al.  Patterns of hypermetria and terminal cocontraction during point-to-point movements demonstrate independent action of trajectory and postural controllers. , 2011, Journal of neurophysiology.

[55]  S. Gielen,et al.  A quantitative analysis of generation of saccadic eye movements by burst neurons. , 1981, Journal of neurophysiology.

[56]  S. Highstein,et al.  Anatomy and physiology of saccadic burst neurons in the alert squirrel monkey. I. Excitatory burst neurons , 1986, The Journal of comparative neurology.

[57]  K. Cullen,et al.  Quantitative analysis of abducens neuron discharge dynamics during saccadic and slow eye movements. , 1999, Journal of neurophysiology.

[58]  R. Leigh,et al.  The neurology of eye movements , 1984 .

[59]  David A. Robinson,et al.  Models of the saccadic eye movement control system , 1973, Kybernetik.

[60]  R. L. Sainburg,et al.  Motor lateralization is characterized by a serial hybrid control scheme , 2011, Neuroscience.

[61]  D. Robinson The mechanics of human saccadic eye movement , 1964, The Journal of physiology.

[62]  R. Shadmehr,et al.  The intrinsic value of visual information affects saccade velocities , 2009, Experimental Brain Research.

[63]  A. Georgopoulos,et al.  The motor cortex and the coding of force. , 1992, Science.

[64]  T. Stein,et al.  Intermanual transfer characteristics of dynamic learning: direction, coordinate frame, and consolidation of interlimb generalization. , 2015, Journal of neurophysiology.

[65]  H C Kwan,et al.  Spatial organization of precentral cortex in awake primates. II. Motor outputs. , 1978, Journal of neurophysiology.

[66]  D. Hoffman,et al.  Corticomotoneuronal cells are “functionally tuned” , 2015, Science.

[67]  Robert L. Sainburg,et al.  Lateralization of motor adaptation reveals independence in control of trajectory and steady-state position , 2007, Experimental Brain Research.

[68]  E. Eldred,et al.  The occurrence of muscle spindles in extraocular muscles of various vertebrates , 1974, Journal of morphology.

[69]  R. Shadmehr,et al.  Cerebellar Contributions to Adaptive Control of Saccades in Humans , 2009, The Journal of Neuroscience.

[70]  Thomas R. Reppert,et al.  Evidence for Hyperbolic Temporal Discounting of Reward in Control of Movements , 2012, The Journal of Neuroscience.

[71]  Aaron L. Wong,et al.  Keeping Your Head On Target , 2013, The Journal of Neuroscience.

[72]  D. Zee,et al.  Effects of ablation of flocculus and paraflocculus of eye movements in primate. , 1981, Journal of neurophysiology.

[73]  Robert L. Sainburg,et al.  Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy , 2009, Neuropsychologia.

[74]  L. Optican,et al.  Cerebellar-dependent adaptive control of primate saccadic system. , 1980, Journal of neurophysiology.

[75]  A. Fuchs,et al.  Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. , 1992, Journal of neurophysiology.

[76]  J Douglas Crawford,et al.  Cervical dystonia: a neural integrator disorder. , 2016, Brain : a journal of neurology.

[77]  Neeraj J Gandhi,et al.  Studies of the Role of the Paramedian Pontine Reticular Formation in the Control of Head‐Restrained and Head‐Unrestrained Gaze Shifts , 2002, Annals of the New York Academy of Sciences.

[78]  Aristides B. Arrenberg,et al.  Spatial gradients and multidimensional dynamics in a neural integrator circuit , 2011, Nature Neuroscience.

[79]  D. Sparks,et al.  Eye movements induced by pontine stimulation: interaction with visually triggered saccades. , 1987, Journal of neurophysiology.

[80]  B. Cohen,et al.  Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways. , 1972, Experimental neurology.

[81]  P. Strick,et al.  Muscle representation in the macaque motor cortex: an anatomical perspective. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[82]  Karolina M. Lempert,et al.  Modulation of Saccade Vigor during Value-Based Decision Making , 2015, The Journal of Neuroscience.

[83]  C. Kaneko,et al.  Eye movement deficits after ibotenic acid lesions of the nucleus prepositus hypoglossi in monkeys. I. Saccades and fixation. , 1997, Journal of neurophysiology.

[84]  A. Fuchs,et al.  Characteristics of saccadic gain adaptation in rhesus macaques. , 1997, Journal of neurophysiology.