A striatal interneuron circuit for continuous target pursuit

Most adaptive behaviors require precise tracking of targets in space. In pursuit behavior with a moving target, mice use distance to target to guide their own movement continuously. Here, we show that in the sensorimotor striatum, parvalbumin-positive fast-spiking interneurons (FSIs) can represent the distance between self and target during pursuit behavior, while striatal projection neurons (SPNs), which receive FSI projections, can represent self-velocity. FSIs are shown to regulate velocity-related SPN activity during pursuit, so that movement velocity is continuously modulated by distance to target. Moreover, bidirectional manipulation of FSI activity can selectively disrupt performance by increasing or decreasing the self-target distance. Our results reveal a key role of the FSI-SPN interneuron circuit in pursuit behavior and elucidate how this circuit implements distance to velocity transformation required for the critical underlying computation.Many natural behaviours involve tracking of a target in space. Here, the authors describe a task to assess this behaviour in mice and use in vivo electrophysiology, calcium imaging, optogenetics, and chemogenetics to investigate the role of the striatum in target pursuit.

[1]  Henry H. Yin,et al.  The role of opponent basal ganglia outputs in behavior , 2016 .

[2]  Feng Zhang,et al.  Channelrhodopsin-2 and optical control of excitable cells , 2006, Nature Methods.

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

[4]  B. Roth,et al.  Evolving the lock to fit the key to create a family of G protein-coupled receptors potently activated by an inert ligand , 2007, Proceedings of the National Academy of Sciences.

[5]  Joseph W. Barter,et al.  Basal Ganglia Outputs Map Instantaneous Position Coordinates during Behavior , 2015, The Journal of Neuroscience.

[6]  Feng Zhang,et al.  Multimodal fast optical interrogation of neural circuitry , 2007, Nature.

[7]  Johannes D. Seelig,et al.  Angular velocity integration in a fly heading circuit , 2017, eLife.

[8]  Garret D Stuber,et al.  Construction of implantable optical fibers for long-term optogenetic manipulation of neural circuits , 2011, Nature Protocols.

[9]  G. Feng,et al.  Learning From Animal Models of Obsessive-Compulsive Disorder , 2015, Biological Psychiatry.

[10]  David Pfau,et al.  Simultaneous Denoising, Deconvolution, and Demixing of Calcium Imaging Data , 2016, Neuron.

[11]  Joshua D. Berke,et al.  Fast-Spiking Interneurons Supply Feedforward Control of Bursting, Calcium, and Plasticity for Efficient Learning , 2018, Cell.

[12]  J. Bolam,et al.  Synaptic organisation of the basal ganglia , 2000, Journal of anatomy.

[13]  Phill-Seung Lee,et al.  Medial preoptic circuit induces hunting-like actions to target objects and prey , 2018, Nature Neuroscience.

[14]  Hao Li,et al.  Optogenetic Editing Reveals the Hierarchical Organization of Learned Action Sequences , 2018, Cell.

[15]  Joseph W. Barter,et al.  Beyond reward prediction errors: the role of dopamine in movement kinematics , 2015, Front. Integr. Neurosci..

[16]  J. Paul Bolam,et al.  Cortical and Thalamic Innervation of Direct and Indirect Pathway Medium-Sized Spiny Neurons in Mouse Striatum , 2010, The Journal of Neuroscience.

[17]  Henry H. Yin,et al.  Bidirectional Modulation of Substantia Nigra Activity by Motivational State , 2013, PloS one.

[18]  M. D. Crutcher,et al.  Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[19]  L. Paninski,et al.  The Spatiotemporal Organization of the Striatum Encodes Action Space , 2017, Neuron.

[20]  R. Krauzlis Recasting the smooth pursuit eye movement system. , 2004, Journal of neurophysiology.

[21]  Joseph W. Barter,et al.  The role of the substantia nigra in posture control , 2014, The European journal of neuroscience.

[22]  C. Gerfen,et al.  CHAPTER 18 – Basal Ganglia , 2004 .

[23]  A. Gamal,et al.  Miniaturized integration of a fluorescence microscope , 2011, Nature Methods.

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

[25]  Venkatesh Saligrama,et al.  Unique contributions of parvalbumin and cholinergic interneurons in organizing striatal networks during movement , 2019, Nature Neuroscience.

[26]  Charles J. Wilson,et al.  Chapter II The basal ganglia , 1996 .

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

[28]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[29]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[30]  Kristen K. Ade,et al.  An Improved BAC Transgenic Fluorescent Reporter Line for Sensitive and Specific Identification of Striatonigral Medium Spiny Neurons , 2011, Front. Syst. Neurosci..

[31]  J. Tepper,et al.  Heterogeneity and Diversity of Striatal GABAergic Interneurons , 2010, Front. Neuroanat..

[32]  J. Deniau,et al.  Synaptic Convergence of Motor and Somatosensory Cortical Afferents onto GABAergic Interneurons in the Rat Striatum , 2002, Journal of Neuroscience.

[33]  E. J. Morris,et al.  Visual motion processing and sensory-motor integration for smooth pursuit eye movements. , 1987, Annual review of neuroscience.

[34]  Liam Paninski,et al.  Efficient and accurate extraction of in vivo calcium signals from microendoscopic video data , 2016, eLife.

[35]  Henry H. Yin,et al.  Striatal firing rate reflects head movement velocity , 2014, The European journal of neuroscience.

[36]  O. Yizhar,et al.  High-efficiency optogenetic silencing with soma-targeted anion-conducting channelrhodopsins , 2017, Nature Communications.

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

[38]  Justin K. O’Hare,et al.  Striatal fast-spiking interneurons selectively modulate circuit output and are required for habitual behavior , 2017, eLife.

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

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

[41]  N. Canteras,et al.  Integrated Control of Predatory Hunting by the Central Nucleus of the Amygdala , 2017, Cell.

[42]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[43]  Henry H Yin,et al.  Striatonigral control of movement velocity in mice , 2016, The European journal of neuroscience.

[44]  P. Rueda-Orozco,et al.  The striatum multiplexes contextual and kinematic information to constrain motor habits execution , 2014, Nature Neuroscience.

[45]  S. Panzeri,et al.  Excitatory GABAergic effects in striatal projection neurons. , 2006, Journal of neurophysiology.

[46]  George Paxinos,et al.  The Mouse Brain in Stereotaxic Coordinates , 2001 .

[47]  Jennifer J. Pokorny,et al.  Activity of substantia nigra pars reticulata neurons during smooth pursuit eye movements in monkeys , 2005, The European journal of neuroscience.

[48]  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.

[49]  Eric A. Yttri,et al.  Opponent and bidirectional control of movement velocity in the basal ganglia , 2016, Nature.

[50]  H. Yin The Basal Ganglia in Action , 2017, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[51]  Minmin Luo,et al.  Hypothalamic Circuits for Predation and Evasion , 2018, Neuron.

[52]  Alan C. Evans,et al.  Functional neuroanatomy of smooth pursuit and predictive saccades , 2000, Neuroreport.

[53]  H. Yin How Basal Ganglia Outputs Generate Behavior , 2014 .

[54]  William Wisden,et al.  Parvalbumin-positive CA1 interneurons are required for spatial working but not for reference memory , 2011, Nature Neuroscience.

[55]  M. DiFiglia,et al.  Altered parvalbumin-positive neuron distribution in basal ganglia of individuals with Tourette syndrome. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[56]  G. Kirouac,et al.  GABAergic projection from the ventral tegmental area and substantia nigra to the periaqueductal gray region and the dorsal raphe nucleus , 2004, The Journal of comparative neurology.

[57]  G. Feng,et al.  Optogenetic Stimulation of Lateral Orbitofronto-Striatal Pathway Suppresses Compulsive Behaviors , 2013, Science.

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

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

[60]  F. Benfenati,et al.  Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin , 1992, Nature.

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

[62]  Alcino J. Silva,et al.  A shared neural ensemble links distinct contextual memories encoded close in time , 2016, Nature.

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

[64]  Anatol C. Kreitzer,et al.  Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry , 2010, Nature.