Role of rodent secondary motor cortex in value-based action selection

Despite widespread neural activity related to reward values, signals related to upcoming choice have not been clearly identified in the rodent brain. Here we examined neuronal activity in the lateral (AGl) and medial (AGm) agranular cortex, corresponding to the primary and secondary motor cortex, respectively, in rats performing a dynamic foraging task. Choice signals, before behavioral manifestation of the rat's choice, arose in the AGm earlier than in any other areas of the rat brain previously studied under free-choice conditions. The AGm also conveyed neural signals for decision value and chosen value. By contrast, upcoming choice signals arose later, and value signals were weaker, in the AGl. We also found that AGm lesions made the rats' choices less dependent on dynamically updated values. These results suggest that rodent secondary motor cortex might be uniquely involved in both representing and reading out value signals for flexible action selection.

[1]  G. Quirk,et al.  The organization of the rat motor cortex: A microstimulation mapping study , 1986, Brain Research Reviews.

[2]  L. Swanson.  The Rat Brain in Stereotaxic Coordinates, George Paxinos, Charles Watson (Eds.). Academic Press, San Diego, CA (1982), vii + 153, $35.00, ISBN: 0 125 47620 5 , 1984 .

[3]  C. Padoa-Schioppa,et al.  Neurons in the orbitofrontal cortex encode economic value , 2006, Nature.

[4]  Daeyeol Lee,et al.  Behavioral and Neural Changes after Gains and Losses of Conditioned Reinforcers , 2009, The Journal of Neuroscience.

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

[6]  Jung Hoon Sul,et al.  Distinct Roles of Rodent Orbitofrontal and Medial Prefrontal Cortex in Decision Making , 2010, Neuron.

[7]  J. Tanji.  The supplementary motor area in the cerebral cortex , 1994, Neuroscience Research.

[8]  Daeyeol Lee,et al.  Encoding of action history in the rat ventral striatum. , 2007, Journal of neurophysiology.

[9]  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.

[10]  Bijan Pesaran,et al.  Free choice activates a decision circuit between frontal and parietal cortex , 2008, Nature.

[11]  Michael L. Platt,et al.  Neural correlates of decision variables in parietal cortex , 1999, Nature.

[12]  H. Uylings,et al.  Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. , 1990, Progress in brain research.

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

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

[15]  J. Tanji,et al.  Distinctions between dorsal and ventral premotor areas: anatomical connectivity and functional properties , 2007, Current Opinion in Neurobiology.

[16]  R. T. Watson,et al.  Efferent Connections of the Rostral Portion of Medial Agranular Cortex in Rats , 1987, Brain Research Bulletin.

[17]  R. Reep,et al.  Topographic organization in the corticocortical connections of medial agranular cortex in rats , 1990, The Journal of comparative neurology.

[18]  Atsutaka Hashimoto,et al.  Afferent connections of medial precentral cortex in the rat , 1984, Neuroscience Letters.

[19]  H. Seo,et al.  Temporal Filtering of Reward Signals in the Dorsal Anterior Cingulate Cortex during a Mixed-Strategy Game , 2007, The Journal of Neuroscience.

[20]  M. Jung,et al.  Fast spiking and regular spiking neural correlates of fear conditioning in the medial prefrontal cortex of the rat. , 2001, Cerebral cortex.

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

[22]  Daeyeol Lee,et al.  Order-Dependent Modulation of Directional Signals in the Supplementary and Presupplementary Motor Areas , 2007, The Journal of Neuroscience.

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

[24]  D. Buxton,et al.  Differential sites of origin and collateralization of corticospinal neurons in the rat: a multiple fluorescent retrograde tracer study , 1992, Brain Research.

[25]  H. Seo,et al.  Lateral Intraparietal Cortex and Reinforcement Learning during a Mixed-Strategy Game , 2009, Journal of Neuroscience.

[26]  W. Kargo,et al.  Adaptation of Prefrontal Cortical Firing Patterns and Their Fidelity to Changes in Action–Reward Contingencies , 2007, The Journal of Neuroscience.

[27]  R. Passingham,et al.  Premotor cortex in the rat. , 1988, Behavioral neuroscience.

[28]  O. Hikosaka,et al.  Visual and Anticipatory Bias in Three Cortical Eye Fields of the Monkey during an Adaptive Decision-Making Task , 2002, The Journal of Neuroscience.

[29]  J M Hinson,et al.  Optimal choice. , 1981, Journal of the experimental analysis of behavior.

[30]  S. Wise,et al.  The motor cortex of the rat: Cytoarchitecture and microstimulation mapping , 1982, The Journal of comparative neurology.

[31]  Namjung Huh,et al.  Model-based reinforcement learning under concurrent schedules of reinforcement in rodents. , 2009, Learning & memory.

[32]  M. Roesch,et al.  Impact of expected reward on neuronal activity in prefrontal cortex, frontal and supplementary eye fields and premotor cortex. , 2003, Journal of neurophysiology.

[33]  M. Roesch,et al.  Orbitofrontal cortex, decision-making and drug addiction , 2006, Trends in Neurosciences.

[34]  D. Barraclough,et al.  Prefrontal cortex and decision making in a mixed-strategy game , 2004, Nature Neuroscience.

[35]  R. Rescorla,et al.  A theory of Pavlovian conditioning : Variations in the effectiveness of reinforcement and nonreinforcement , 1972 .

[36]  Kenway Louie,et al.  Separating Value from Choice: Delay Discounting Activity in the Lateral Intraparietal Area , 2010, The Journal of Neuroscience.

[37]  M. Miller,et al.  The origin of corticospinal projection neurons in rat , 2004, Experimental Brain Research.

[38]  M. Dorris,et al.  Role of the Superior Colliculus in Choosing Mixed-Strategy Saccades , 2009, The Journal of Neuroscience.

[39]  Jonathan D. Wallis,et al.  Neurons in the Frontal Lobe Encode the Value of Multiple Decision Variables , 2009, Journal of Cognitive Neuroscience.

[40]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[41]  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 .

[42]  A. Cooper,et al.  Predictive Reward Signal of Dopamine Neurons , 2011 .

[43]  K. Kurata,et al.  Quantitative analyses of thalamic and cortical origins of neurons projecting to the rostral and caudal forelimb motor areas in the cerebral cortex of rats , 1998, Brain Research.

[44]  M. Roesch,et al.  Neuronal Activity Related to Reward Value and Motivation in Primate Frontal Cortex , 2004, Science.

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

[46]  M. Roesch,et al.  Encoding of Time-Discounted Rewards in Orbitofrontal Cortex Is Independent of Value Representation , 2006, Neuron.

[47]  M. Jung,et al.  Dynamics of Population Code for Working Memory in the Prefrontal Cortex , 2003, Neuron.

[48]  J. Donoghue,et al.  Afferent connections of the lateral agranular field of the rat motor cortex , 1983, The Journal of comparative neurology.

[49]  W. Newsome,et al.  Matching Behavior and the Representation of Value in the Parietal Cortex , 2004, Science.

[50]  C. Kennard,et al.  Functional role of the supplementary and pre-supplementary motor areas , 2008, Nature Reviews Neuroscience.

[51]  K. Sanderson,et al.  Reevaluation of motor cortex and of sensorimotor overlap in cerebral cortex of albino rats , 1984, Brain Research.