Striatal firing rate reflects head movement velocity

Although the basal ganglia have long been implicated in the initiation of actions, their contribution to movement remains a matter of dispute. Using wireless multi‐electrode recording and motion tracking, we examined the relationship between single‐unit activity in the sensorimotor striatum and movement kinematics. We recorded single‐unit activity from medium spiny projection neurons and fast‐spiking interneurons while monitoring the movements of mice using motion tracking. In Experiment 1, we trained mice to generate movements reliably by water‐depriving them and giving them periodic cued sucrose rewards. We found high correlations between single‐unit activity and movement velocity in particular directions. This correlation was found in both putative medium spiny projection neurons and fast‐spiking interneurons. In Experiment 2, to rule out the possibility that the observed correlations were due to reward expectancy, we repeated the same procedure but added trials in which sucrose delivery was replaced by an aversive air puff stimulus. The air puff generated avoidance movements that were clearly different from movements on rewarded trials, but the same neurons that showed velocity correlation on reward trials exhibited a similar correlation on air puff trials. These experiments show for the first time that the firing rate of striatal neurons reflects movement velocity for different types of movements, whether to seek rewards or to avoid harm.

[1]  Minmin Luo,et al.  Pharmacogenetic activation of midbrain dopaminergic neurons induces hyperactivity , 2013, Neuroscience Bulletin.

[2]  H. Yin,et al.  The role of the basal ganglia in habit formation , 2006, Nature Reviews Neuroscience.

[3]  N. Uchida,et al.  The dorsomedial striatum encodes net expected return, critical for energizing performance vigor , 2013, Nature Neuroscience.

[4]  D. Lovinger,et al.  Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill , 2009, Nature Neuroscience.

[5]  B. D. Bennett,et al.  Synaptic input and output of parvalbumin-immunoreactive neurons in the neostriatum of the rat , 1994, Neuroscience.

[6]  H. Yin The Sensorimotor Striatum Is Necessary for Serial Order Learning , 2010, The Journal of Neuroscience.

[7]  A. Sadikot,et al.  Thalamic input to parvalbumin-immunoreactive GABAergic interneurons: organization in normal striatum and effect of neonatal decortication , 1999, Neuroscience.

[8]  R. Tomlinson,et al.  Ocular motor deficits in Parkinson's disease. II. Control of the saccadic and smooth pursuit systems. , 1983, Brain : a journal of neurology.

[9]  M. Roesch,et al.  Reward Prediction Error Signaling in Posterior Dorsomedial Striatum Is Action Specific , 2012, The Journal of Neuroscience.

[10]  C. Gerfen,et al.  The neostriatal mosaic: compartmental distribution of calcium-binding protein and parvalbumin in the basal ganglia of the rat and monkey. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. D. Crutcher,et al.  Single cell studies of the primate putamen , 2004, Experimental Brain Research.

[12]  Stanislav Herwik,et al.  A Wireless Multi-Channel Recording System for Freely Behaving Mice and Rats , 2011, PloS one.

[13]  K. Abe,et al.  Motor neglect following left thalamic hemorrhage: a case report , 1999, Journal of the Neurological Sciences.

[14]  B. Balleine,et al.  Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning , 2004, The European journal of neuroscience.

[15]  D. Robinson,et al.  Integrating with neurons. , 1989, Annual review of neuroscience.

[16]  J. Mink,et al.  Recent advances in Tourette syndrome research , 2006, Trends in Neurosciences.

[17]  Thomas A. McMahon,et al.  Muscles, Reflexes, and Locomotion , 1984 .

[18]  C. Marsden,et al.  Stereotyped behaviour patterns and hyperactivity induced by amphetamine and apomorphine after discrete 6-hydroxydopamine lesions of extrapyramidal and mesolimbic nuclei , 1977, Brain Research.

[19]  H. Miller The Basal Ganglia and Posture , 1968 .

[20]  Xin Jin,et al.  Basal Ganglia Subcircuits Distinctively Encode the Parsing and Concatenation of Action Sequences , 2014, Nature Neuroscience.

[21]  Y. Isomura,et al.  Reward-Modulated Motor Information in Identified Striatum Neurons , 2013, The Journal of Neuroscience.

[22]  J. Eccles,et al.  The action of tetanus toxin on the inhibition of motoneurones , 1957, The Journal of physiology.

[23]  R. Mark Wightman,et al.  Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter , 1996, Nature.

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

[25]  W. Schultz,et al.  Reward-related activity in the monkey striatum and substantia nigra. , 1993, Progress in brain research.

[26]  Rui M. Costa,et al.  Rapid Alterations in Corticostriatal Ensemble Coordination during Acute Dopamine-Dependent Motor Dysfunction , 2006, Neuron.

[27]  Miguel A. L. Nicolelis,et al.  Methods for Neural Ensemble Recordings , 1998 .

[28]  M. Nicolelis,et al.  Differential Corticostriatal Plasticity during Fast and Slow Motor Skill Learning in Mice , 2004, Current Biology.

[29]  N. Mallet,et al.  Relationships between the Firing of Identified Striatal Interneurons and Spontaneous and Driven Cortical Activities In Vivo , 2012, The Journal of Neuroscience.

[30]  A. A. Skavenski,et al.  Role of abducens neurons in vestibuloocular reflex. , 1973, Journal of neurophysiology.

[31]  A. Fuchs,et al.  The neuronal substrate of integration in the oculomotor system , 1992, Progress in Neurobiology.

[32]  Anatol C. Kreitzer,et al.  Selective Inhibition of Striatal Fast-Spiking Interneurons Causes Dyskinesias , 2011, The Journal of Neuroscience.

[33]  J. Marshall,et al.  Striatal dopamine and glutamate receptors modulate methamphetamine-induced cortical Fos expression , 2009, Neuroscience.

[34]  W. Schultz,et al.  Neuronal activity in the monkey striatum during the initiation of movements , 2004, Experimental Brain Research.

[35]  Henry H Yin,et al.  Action, time and the basal ganglia , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[36]  O. Hikosaka,et al.  Functional properties of monkey caudate neurons. I. Activities related to saccadic eye movements. , 1989, Journal of neurophysiology.

[37]  Henrike Planert,et al.  Dynamics of Synaptic Transmission between Fast-Spiking Interneurons and Striatal Projection Neurons of the Direct and Indirect Pathways , 2010, The Journal of Neuroscience.

[38]  M. Hallett,et al.  Pathophysiology of bradykinesia in Parkinson's disease. , 2001, Brain : a journal of neurology.

[39]  M. West,et al.  Distributions of single neurons related to body parts in the lateral striatum of the rat , 1997, Brain Research.

[40]  G. Krauthamer,et al.  Somatosensory neurons projecting from the superior colliculus to the intralaminar thalamus in the rat , 1990, Brain Research.

[41]  B. Balleine,et al.  The role of the dorsomedial striatum in instrumental conditioning , 2005, The European journal of neuroscience.

[42]  David Fan,et al.  Mechanisms of Action Selection and Timing in Substantia Nigra Neurons , 2012, The Journal of Neuroscience.

[43]  Steven S. Vogel,et al.  Concurrent Activation of Striatal Direct and Indirect Pathways During Action Initiation , 2013, Nature.

[44]  Anatol C. Kreitzer,et al.  Striatal microcircuitry and movement disorders , 2012, Trends in Neurosciences.

[45]  Stéphane Charpier,et al.  Feedforward Inhibition of Projection Neurons by Fast-Spiking GABA Interneurons in the Rat Striatum In Vivo , 2005, The Journal of Neuroscience.

[46]  A. Sadikot,et al.  GABA promotes survival but not proliferation of parvalbumin-immunoreactive interneurons in rodent neostriatum: an in vivo study with stereology , 2001, Neuroscience.

[47]  O. Hikosaka,et al.  Expectation of reward modulates cognitive signals in the basal ganglia , 1998, Nature Neuroscience.

[48]  O. Hikosaka,et al.  Feature-Based Anticipation of Cues that Predict Reward in Monkey Caudate Nucleus , 2002, Neuron.

[49]  Scott T. Grafton,et al.  Motor subcircuits mediating the control of movement extent and speed. , 2003, Journal of neurophysiology.

[50]  H. Yin Cortico-Basal Ganglia Networks and the Neural Substrates of Actions , 2014 .

[51]  M. Marinelli,et al.  Dopamine Scales Performance in the Absence of New Learning , 2006, Neuron.

[52]  G. E. Alexander,et al.  Functional architecture of basal ganglia circuits: neural substrates of parallel processing , 1990, Trends in Neurosciences.

[53]  M. D. Crutcher,et al.  Single cell studies of the primate putamen , 2004, Experimental Brain Research.

[54]  J. Mink THE BASAL GANGLIA: FOCUSED SELECTION AND INHIBITION OF COMPETING MOTOR PROGRAMS , 1996, Progress in Neurobiology.

[55]  C. Gerfen The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. , 1992, Annual review of neuroscience.

[56]  Garrett E. Alexander Basal ganglia , 1998 .

[57]  L. Crespi Amount of reinforcement and level of performance. , 1944 .

[58]  M. Desmurget,et al.  Basal ganglia contributions to motor control: a vigorous tutor , 2010, Current Opinion in Neurobiology.

[59]  C. Saper,et al.  Decreased number of parvalbumin and cholinergic interneurons in the striatum of individuals with Tourette syndrome , 2010, The Journal of comparative neurology.

[60]  Peter Redgrave,et al.  Basal Ganglia , 2020, Encyclopedia of Autism Spectrum Disorders.

[61]  Joshua D. Berke,et al.  Functional Properties of Striatal Fast-Spiking Interneurons , 2011, Front. Syst. Neurosci..

[62]  G. Shepherd The Synaptic Organization of the Brain , 1979 .

[63]  H. Yin,et al.  The Role of Mediodorsal Thalamus in Temporal Differentiation of Reward-Guided Actions , 2010, Front. Integr. Neurosci..

[64]  Miguel A. L. Nicolelis Methods for Neural Ensemble Recordings, Second Edition , 2007 .

[65]  Alexander B. Wiltschko,et al.  Selective Activation of Striatal Fast-Spiking Interneurons during Choice Execution , 2010, Neuron.

[66]  H. Yin,et al.  Dynamic Changes in Single Unit Activity and Gamma Oscillations in a Thalamocortical Circuit during Rapid Instrumental Learning , 2012, PloS one.

[67]  W. Smith The Integrative Action of the Nervous System , 1907, Nature.

[68]  Anatol C. Kreitzer,et al.  Distinct Roles of GABAergic Interneurons in the Regulation of Striatal Output Pathways , 2010, The Journal of Neuroscience.

[69]  S. Iversen,et al.  Sensorimotor impairments following localized kainic acid and 6-hydroxydopamine lesions of the neostriatum , 1982, Brain Research.