Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action value

In changing environments, animals must adaptively select actions to achieve their goals. In tasks involving goal-directed action selection, striatal neural activity has been shown to represent the value of competing actions. Striatal representations of action value could potentially bias responses toward actions of higher value. However, no study to date has demonstrated the direct effect of distinct striatal pathways in goal-directed action selection. We found that transient optogenetic stimulation of dorsal striatal dopamine D1 and D2 receptor–expressing neurons during decision-making in mice introduced opposing biases in the distribution of choices. The effect of stimulation on choice was dependent on recent reward history and mimicked an additive change in the action value. Although stimulation before and during movement initiation produced a robust bias in choice behavior, this bias was substantially diminished when stimulation was delayed after response initiation. Together, our data suggest that striatal activity is involved in goal-directed action selection.

[1]  J. Oller,et al.  Consensus and controversy , 1984 .

[2]  J. Penney,et al.  The functional anatomy of basal ganglia disorders , 1989, Trends in Neurosciences.

[3]  William T. Newsome,et al.  Cortical microstimulation influences perceptual judgements of motion direction , 1990, Nature.

[4]  M. Delong,et al.  Primate models of movement disorders of basal ganglia origin , 1990, Trends in Neurosciences.

[5]  C. Gerfen The neostriatal mosaic: multiple levels of compartmental organization , 1992, Trends in Neurosciences.

[6]  Charles J. Wilson,et al.  Striatal interneurones: chemical, physiological and morphological characterization , 1995, Trends in Neurosciences.

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

[8]  J. P. Huston,et al.  The unilateral 6-hydroxydopamine lesion model in behavioral brain research. Analysis of functional deficits, recovery and treatments , 1996, Progress in Neurobiology.

[9]  Peter Dayan,et al.  A Neural Substrate of Prediction and Reward , 1997, Science.

[10]  P. Redgrave,et al.  Is the short-latency dopamine response too short to signal reward error? , 1999, Trends in Neurosciences.

[11]  P. Redgrave,et al.  The basal ganglia: a vertebrate solution to the selection problem? , 1999, Neuroscience.

[12]  A. Doupe,et al.  Interruption of a basal ganglia–forebrain circuit prevents plasticity of learned vocalizations , 2000, Nature.

[13]  O. Hikosaka,et al.  A neural correlate of response bias in monkey caudate nucleus , 2002, Nature.

[14]  B. Stein,et al.  Opposing basal ganglia processes shape midbrain visuomotor activity bilaterally , 2003, Nature.

[15]  Wolfram Schultz,et al.  Effects of expectations for different reward magnitudes on neuronal activity in primate striatum. , 2003, Journal of neurophysiology.

[16]  Okihide Hikosaka,et al.  Reward-Dependent Gain and Bias of Visual Responses in Primate Superior Colliculus , 2003, Neuron.

[17]  A. Sadikot,et al.  Neurogenesis and stereological morphometry of calretinin‐immunoreactive GABAergic interneurons of the neostriatum , 2004, The Journal of comparative neurology.

[18]  A. Graybiel,et al.  Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories , 2005, Nature.

[19]  K. Doya,et al.  Representation of Action-Specific Reward Values in the Striatum , 2005, Science.

[20]  E. Miller,et al.  Different time courses of learning-related activity in the prefrontal cortex and striatum , 2005, Nature.

[21]  S. Grillner,et al.  Mechanisms for selection of basic motor programs – roles for the striatum and pallidum , 2005, Trends in Neurosciences.

[22]  Richard S. Sutton,et al.  Reinforcement Learning: An Introduction , 1998, IEEE Trans. Neural Networks.

[23]  W. Newsome,et al.  Choosing the greater of two goods: neural currencies for valuation and decision making , 2005, Nature Reviews Neuroscience.

[24]  O. Hikosaka,et al.  Immediate changes in anticipatory activity of caudate neurons associated with reversal of position-reward contingency. , 2005, Journal of neurophysiology.

[25]  P. Glimcher,et al.  JOURNAL OF THE EXPERIMENTAL ANALYSIS OF BEHAVIOR 2005, 84, 555–579 NUMBER 3(NOVEMBER) DYNAMIC RESPONSE-BY-RESPONSE MODELS OF MATCHING BEHAVIOR IN RHESUS MONKEYS , 2022 .

[26]  Scott H Chandler,et al.  Striatal potassium channel dysfunction in Huntington's disease transgenic mice. , 2005, Journal of neurophysiology.

[27]  Kae Nakamura,et al.  Basal ganglia orient eyes to reward. , 2006, Journal of neurophysiology.

[28]  Xiao-Jing Wang,et al.  Cortico–basal ganglia circuit mechanism for a decision threshold in reaction time tasks , 2006, Nature Neuroscience.

[29]  B. Balleine,et al.  The Role of the Dorsal Striatum in Reward and Decision-Making , 2007, The Journal of Neuroscience.

[30]  J. Gold,et al.  The neural basis of decision making. , 2007, Annual review of neuroscience.

[31]  Charles R. Gerfen,et al.  Targeting Cre Recombinase to Specific Neuron Populations with Bacterial Artificial Chromosome Constructs , 2007, The Journal of Neuroscience.

[32]  M. Ragozzino The Contribution of the Medial Prefrontal Cortex, Orbitofrontal Cortex, and Dorsomedial Striatum to Behavioral Flexibility , 2007, Annals of the New York Academy of Sciences.

[33]  S. Grillner,et al.  Neural bases of goal-directed locomotion in vertebrates—An overview , 2008, Brain Research Reviews.

[34]  Colin Camerer,et al.  A framework for studying the neurobiology of value-based decision making , 2008, Nature Reviews Neuroscience.

[35]  Anatol C. Kreitzer,et al.  Striatal Plasticity and Basal Ganglia Circuit Function , 2008, Neuron.

[36]  B. Gloss,et al.  Drd1a-tdTomato BAC Transgenic Mice for Simultaneous Visualization of Medium Spiny Neurons in the Direct and Indirect Pathways of the Basal Ganglia , 2008, The Journal of Neuroscience.

[37]  P. Glimcher,et al.  Value Representations in the Primate Striatum during Matching Behavior , 2008, Neuron.

[38]  Gidon Felsen,et al.  Neural Substrates of Sensory-Guided Locomotor Decisions in the Rat Superior Colliculus , 2008, Neuron.

[39]  Mark Laubach,et al.  The Dorsomedial Striatum Reflects Response Bias during Learning , 2009, The Journal of Neuroscience.

[40]  A. Graybiel,et al.  Stable encoding of task structure coexists with flexible coding of task events in sensorimotor striatum. , 2009, Journal of neurophysiology.

[41]  P. Glimcher,et al.  The Neurobiology of Decision: Consensus and Controversy , 2009, Neuron.

[42]  Jung Hoon Sul,et al.  Role of Striatum in Updating Values of Chosen Actions , 2009, The Journal of Neuroscience.

[43]  O. Hikosaka,et al.  Perceptual Learning, Motor Learning and Automaticity Switching from Automatic to Controlled Behavior: Cortico-basal Ganglia Mechanisms , 2022 .

[44]  T. Robbins,et al.  Selective lesions of the dorsomedial striatum impair serial spatial reversal learning in rats , 2010, Behavioural Brain Research.

[45]  Xin Jin,et al.  Start/stop signals emerge in nigrostriatal circuits during sequence learning , 2010, Nature.

[46]  A. Graybiel,et al.  Differential Dynamics of Activity Changes in Dorsolateral and Dorsomedial Striatal Loops during Learning , 2010, Neuron.

[47]  Michel Desmurget,et al.  Motor Sequences and the Basal Ganglia: Kinematics, Not Habits , 2010, The Journal of Neuroscience.

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

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

[50]  E. Nestler,et al.  The Striatal Balancing Act in Drug Addiction: Distinct Roles of Direct and Indirect Pathway Medium Spiny Neurons , 2011, Front. Neuroanat..

[51]  Okihide Hikosaka,et al.  Cortico‐basal ganglia mechanisms for overcoming innate, habitual and motivational behaviors , 2011, The European journal of neuroscience.

[52]  Anatol C. Kreitzer,et al.  Investigating striatal function through cell-type-specific manipulations , 2011, Neuroscience.

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

[54]  Anatol C. Kreitzer,et al.  Distinct roles for direct and indirect pathway striatal neurons in reinforcement , 2012, Nature Neuroscience.