Cognitive control of movement via the cerebellar-recipient thalamus

The cognitive control of behavior was long considered to be centralized in cerebral cortex. More recently, subcortical structures such as cerebellum and basal ganglia have been implicated in cognitive functions as well. The fact that subcortico-cortical circuits for the control of movement involve the thalamus prompts the notion that activity in movement-related thalamus may also reflect elements of cognitive behavior. Yet this hypothesis has rarely been investigated. Using the pathways linking cerebellum to cerebral cortex via the thalamus as a template, we review evidence that the motor thalamus, together with movement-related central thalamus have the requisite connectivity and activity to mediate cognitive aspects of movement control.

[1]  Driss Boussaoud,et al.  Origin of thalamic inputs to the primary, premotor, and supplementary motor cortical areas and to area 46 in macaque monkeys: A multiple retrograde tracing study , 1999, The Journal of comparative neurology.

[2]  P. Strick.  The influence of motor preparation on the response of cerebellar neurons to limb displacements , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[3]  J. Lynch,et al.  Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport , 2004, Experimental Brain Research.

[4]  K. Kalil.  Projections of the cerebellar and dorsal column nuclei upon the thalamus of the rhesus monkey , 1981, The Journal of comparative neurology.

[5]  P. Strick,et al.  Cerebellar Projections to the Prefrontal Cortex of the Primate , 2001, The Journal of Neuroscience.

[6]  Thierry Wannier,et al.  Divergence and convergence of thalamocortical projections to premotor and supplementary motor cortex: a multiple tracing study in the macaque monkey , 2005, The European journal of neuroscience.

[7]  A. Diamond.  Close interrelation of motor development and cognitive development and of the cerebellum and prefrontal cortex. , 2000, Child development.

[8]  T. Powell,et al.  The connexions of the striatum and globus pallidus: synthesis and speculation. , 1971, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  M. S. Salman.  Topical Review : The Cerebellum: It's About Time! But Timing Is Not Everything-New Insights Into the Role of the Cerebellum in Timing Motor and Cognitive Tasks , 2002, Journal of child neurology.

[10]  B. Okuda,et al.  Cerebello-thalamo-cerebral projection from the dentate nucleus onto the frontal eye field in the cat. , 1994, Acta physiologica Scandinavica.

[11]  H. Kuypers,et al.  Organization of the thalamo-cortical connexions to the frontal lobe in the rhesus monkey , 1977, Experimental Brain Research.

[12]  Jonathan D. Nelson,et al.  How Embodied Is Perceptual Decision Making? Evidence for Separate Processing of Perceptual and Motor Decisions , 2013, The Journal of Neuroscience.

[13]  G. Kreiman,et al.  Internally Generated Preactivation of Single Neurons in Human Medial Frontal Cortex Predicts Volition , 2011, Neuron.

[14]  P. Strick,et al.  The cerebellum communicates with the basal ganglia , 2005, Nature Neuroscience.

[15]  P. Strick,et al.  Supplementary Motor Area and Presupplementary Motor Area: Targets of Basal Ganglia and Cerebellar Output , 2007, The Journal of Neuroscience.

[16]  Monica Maranesi,et al.  Neurons Controlling Voluntary Vocalization in the Macaque Ventral Premotor Cortex , 2011, PloS one.

[17]  Marc A Sommer,et al.  The role of the thalamus in motor control , 2003, Current Opinion in Neurobiology.

[18]  P. Strick,et al.  Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. , 1994, Science.

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

[20]  J Schlag,et al.  Primate supplementary eye field. II. Comparative aspects of connections with the thalamus, corpus striatum, and related forebrain nuclei , 1991, The Journal of comparative neurology.

[21]  E. Procyk,et al.  The primate working memory networks , 2004, Cognitive, affective & behavioral neuroscience.

[22]  I. Ilinsky,et al.  Thalamic terminal fields of individual axons from the ventral part of the dentate nucleus of the cerebellum in Macaca mulatta , 2000, The Journal of comparative neurology.

[23]  P. Strick,et al.  Preferential activity of dentate neurons during limb movements guided by vision. , 1993, Journal of neurophysiology.

[24]  M. Giurfa.  Cognition with few neurons: higher-order learning in insects , 2013, Trends in Neurosciences.

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

[26]  Y. Shinoda,et al.  Synaptic organization of the cerebello-thalamo-cerebral pathway in the cat. I. Projection of individual cerebellar nuclei to single pyramidal tract neurons in areas 4 and 6 , 1985, Neuroscience Research.

[27]  G. Percheron,et al.  The primate motor thalamus , 1996, Brain Research Reviews.

[28]  Y. Saalmann,et al.  Cognitive and Perceptual Functions of the Visual Thalamus , 2011, Neuron.

[29]  H. Shibutani,et al.  Chapter 31 Context dependent discharge characteristics of saccade-related Purkinje cells in the cerebellar hemispheres of the monkey , 1996 .

[30]  Christian Bellebaum,et al.  Mechanisms of cerebellar contributions to cognition in humans. , 2012, Wiley interdisciplinary reviews. Cognitive science.

[31]  D. Pandya,et al.  Anatomical investigation of projections from thalamus to posterior parietal cortex in the rhesus monkey: A WGA‐HRP and fluorescent tracer study , 1990, The Journal of comparative neurology.

[32]  G. Rizzolatti,et al.  Thalamic input to inferior area 6 and area 4 in the macaque monkey , 1989, The Journal of comparative neurology.

[33]  M. Witter,et al.  The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness , 2002, Brain Research Reviews.

[34]  Tanaka.  The role of , 2000, Journal of insect physiology.

[35]  S. Aglioti.  THE ROLE OF THE THALAMUS AND BASAL GANGLIA IN HUMAN COGNITION , 1997, Journal of Neurolinguistics.

[36]  Jaime S. Ide,et al.  A cerebellar thalamic cortical circuit for error-related cognitive control , 2011, NeuroImage.

[37]  Masaki Tanaka,et al.  Cognitive Signals in the Primate Motor Thalamus Predict Saccade Timing , 2007, The Journal of Neuroscience.

[38]  J. Olszewski.  The Thalamus of the Macaca Mulatta: An Atlas for Use with the Stereotaxic Instrument , 1952 .

[39]  Robin C. Ashmore,et al.  Delay activity of saccade-related neurons in the caudal dentate nucleus of the macaque cerebellum. , 2013, Journal of neurophysiology.

[40]  W. Graf,et al.  Cerebellar inputs to intraparietal cortex areas LIP and MIP: functional frameworks for adaptive control of eye movements, reaching, and arm/eye/head movement coordination. , 2010, Cerebral cortex.

[41]  A. L. Leiner,et al.  Reappraising the cerebellum: what does the hindbrain contribute to the forebrain? , 1989, Behavioral neuroscience.

[42]  A. L. Leiner,et al.  Does the cerebellum contribute to mental skills? , 1986, Behavioral neuroscience.

[43]  R. Grimm,et al.  The activity of dentate neurons during an arm movement sequence. , 1974, Brain research.

[44]  John E. Desmond,et al.  Temporal dynamics of cerebro-cerebellar network recruitment during a cognitive task , 2005, Neuropsychologia.

[45]  J F Stein,et al.  Neuronal activity in the primate motor thalamus during visually triggered and internally generated limb movements. , 1999, Journal of neurophysiology.

[46]  M. Wiesendanger,et al.  The thalamic connections with medial area 6 (supplementary motor cortex) in the monkey (macaca fascicularis) , 2004, Experimental Brain Research.

[47]  Narender Ramnani,et al.  Frontal Lobe and Posterior Parietal Contributions to the Cortico-cerebellar System , 2011, The Cerebellum.

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

[49]  C. Colby,et al.  Spatial representations for action in parietal cortex. , 1996, Brain research. Cognitive brain research.

[50]  J Schlag,et al.  Visuomotor functions of central thalamus in monkey. I. Unit activity related to spontaneous eye movements. , 1984, Journal of neurophysiology.

[51]  Catherine J. Stoodley,et al.  The Cerebellum and Cognition: Evidence from Functional Imaging Studies , 2011, The Cerebellum.

[52]  M. Schlag-Rey,et al.  Visuomotor functions of central thalamus in monkey. II. Unit activity related to visual events, targeting, and fixation. , 1984, Journal of neurophysiology.

[53]  P. Strick,et al.  Activity of ventrolateral thalamic neurons during arm movement. , 1976, Journal of neurophysiology.

[54]  P S Goldman-Rakic,et al.  Mediodorsal nucleus: Areal, laminar, and tangential distribution of afferents and efferents in the frontal lobe of rhesus monkeys , 1988, The Journal of comparative neurology.

[55]  Jun Tanji,et al.  The relationship between MI and SMA afferents and cerebellar and pallidal efferents in the macaque monkey , 2002, Somatosensory & motor research.

[56]  C. Brunia.  Neural aspects of anticipatory behavior. , 1999, Acta psychologica.

[57]  R. Wurtz,et al.  What the brain stem tells the frontal cortex. II. Role of the SC-MD-FEF pathway in corollary discharge. , 2004, Journal of neurophysiology.

[58]  L. Fadiga,et al.  Active perception: sensorimotor circuits as a cortical basis for language , 2010, Nature Reviews Neuroscience.

[59]  Mark D. Johnson,et al.  The Role of the Human Thalamus in Language and Memory: Evidence from Electrophysiological Studies , 2000, Brain and Cognition.

[60]  S. Haber,et al.  The cortico-basal ganglia integrative network: The role of the thalamus , 2009, Brain Research Bulletin.

[61]  K. Jinnai,et al.  Projection of the cerebellar dentate nucleus onto the frontal association cortex in monkeys , 1979, Experimental Brain Research.

[62]  Masaki Tanaka.  Spatiotemporal properties of eye position signals in the primate central thalamus. , 2007, Cerebral cortex.

[63]  Christian Bellebaum,et al.  Altered Error Processing following Vascular Thalamic Damage: Evidence from an Antisaccade Task , 2011, PloS one.

[64]  J. Lynch,et al.  Subcortical Input to the Smooth and Saccadic Eye Movement Subregions of the Frontal Eye Field in Cebus Monkey , 1997, The Journal of Neuroscience.

[65]  Dottie M. Clower,et al.  Basal ganglia and cerebellar inputs to 'AIP'. , 2005, Cerebral cortex.

[66]  Yusuke Murayama,et al.  Unravelling cerebellar pathways with high temporal precision targeting motor and extensive sensory and parietal networks , 2012, Nature Communications.

[67]  F. Binkofski,et al.  Motor functions of the Broca’s region , 2004, Brain and Language.

[68]  R. Wurtz,et al.  What the brain stem tells the frontal cortex. I. Oculomotor signals sent from superior colliculus to frontal eye field via mediodorsal thalamus. , 2004, Journal of neurophysiology.

[69]  Jun Kunimatsu,et al.  Contribution of the central thalamus to the generation of volitional saccades , 2011, The European journal of neuroscience.

[70]  J. Assad,et al.  A cognitive signal for the proactive timing of action in macaque LIP , 2006, Nature Neuroscience.

[71]  Y. Shinoda,et al.  Two modes of cerebellar input to the parietal cortex in the cat , 2004, Experimental Brain Research.

[72]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.

[73]  M. E. Anderson,et al.  Activity of neurons in cerebellar-receiving and pallidal-receiving areas of the thalamus of the behaving monkey. , 1991, Journal of neurophysiology.

[74]  H. Groenewegen,et al.  The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei , 1994, Trends in Neurosciences.

[75]  Jeremy D. Schmahmann,et al.  The Role of the Cerebellum in Cognition and Emotion: Personal Reflections Since 1982 on the Dysmetria of Thought Hypothesis, and Its Historical Evolution from Theory to Therapy , 2010, Neuropsychology Review.

[76]  W. T. Thach,et al.  Anatomical evidence for segregated focal groupings of efferent cells and their terminal ramifications in the cerebellothalamic pathway of the monkey , 1983, Brain Research Reviews.

[77]  J F Stein,et al.  Temporary inactivation in the primate motor thalamus during visually triggered and internally generated limb movements. , 2000, Journal of neurophysiology.

[78]  M. Schlag-Rey,et al.  The central thalamus. , 1989, Reviews of oculomotor research.

[79]  N. Ichinohe,et al.  A di-synaptic projection from the lateral cerebellar nucleus to the laterodorsal part of the striatum via the central lateral nucleus of the thalamus in the rat , 2000, Brain Research.

[80]  J. Stein,et al.  Role of the cerebellum in the visual guidance of movement. , 1992, Nature.

[81]  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.

[82]  M. Wiesendanger,et al.  Cerebello-cortical linkage in the monkey as revealed by transcellular labeling with the lectin wheat germ agglutinin conjugated to the marker horseradish peroxidase , 2004, Experimental Brain Research.

[83]  Aart J. Nederveen,et al.  Functional MRI study of response inhibition in myoclonus dystonia , 2013, Experimental Neurology.

[84]  G. Knoblich,et al.  Predicting the Effects of Actions: Interactions of Perception and Action , 2001, Psychological science.

[85]  Dana Chidekel,et al.  From Movement to Thought: Executive Function, Embodied Cognition, and the Cerebellum , 2012, The Cerebellum.

[86]  R. Guillery.  Anatomical evidence concerning the role of the thalamus in corticocortical communication: a brief review. , 1995, Journal of anatomy.

[87]  L A Krubitzer,et al.  Frontal eye field as defined by intracortical microstimulation in squirrel monkeys, owl monkeys, and macaque monkeys II. cortical connections , 1986, The Journal of comparative neurology.

[88]  R. Mair,et al.  Cognitive Activation by Central Thalamic Stimulation: The Yerkes-Dodson Law Revisited , 2011, Dose-response : a publication of International Hormesis Society.

[89]  Xiaofeng Lu,et al.  Anatomical evidence for the involvement of medial cerebellar output from the interpositus nuclei in cognitive functions , 2012, Proceedings of the National Academy of Sciences.

[90]  Dottie M. Clower,et al.  The Inferior Parietal Lobule Is the Target of Output from the Superior Colliculus, Hippocampus, and Cerebellum , 2001, The Journal of Neuroscience.

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

[92]  Peter L. Strick,et al.  The Cerebellum and Basal Ganglia are Interconnected , 2010, Neuropsychology Review.

[93]  J. Price,et al.  The organization of projections from the mediodorsal nucleus of the thalamus to orbital and medial prefrontal cortex in macaque monkeys , 1993, The Journal of comparative neurology.

[94]  H. Shibasaki,et al.  Volitional movement is not preceded by cortical slow negativity in cerebellar dentate lesion in man , 1986, Brain Research.

[95]  G. B. Stanton.  Topographical organization of ascending cerebellar projections from the dentate and interposed nuclei in Macaca mulatta: An anterograde degeneration study , 1980, The Journal of comparative neurology.

[96]  A. L. Leiner,et al.  Cognitive and language functions of the human cerebellum , 1993, Trends in Neurosciences.

[97]  W. T. Thach.  Cerebellar inputs to motor cortex. , 1987, Ciba Foundation symposium.

[98]  Nicole Law,et al.  Cerebello–thalamo–cerebral connections in pediatric brain tumor patients: Impact on working memory , 2011, NeuroImage.

[99]  D. Melchitzky,et al.  Subcortical afferents to the lateral mediodorsal thalamus in cynomolgus monkeys , 2004, Neuroscience.

[100]  Stephen E Nadeau,et al.  The thalamus and working memory , 2008, Journal of the International Neuropsychological Society.

[101]  P. Goldman-Rakic,et al.  Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: evidence for a distributed neural network subserving spatially guided behavior , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.