The basal ganglia, the ideal machinery for the cost-benefit analysis of action plans

Basal ganglia dysfunction causes profound movement disorders, often attributed to imbalance between direct and indirect pathway activity in the sensorimotor basal ganglia. In the classical view, the direct pathway facilitates movements, whereas the indirect pathway inhibits movements. However, the recent finding of co-activation of the two pathways during movement challenges this view. Reconciling the new finding with the body of evidence supporting the classical view, this perspective proposes that the direct pathway computes the expected benefits of motor plans entering the basal ganglia, while the indirect pathway computes their expected costs. Thus, basal ganglia output combining the two pathway signals in a subtraction manner weighs benefits against costs, and endorses the plan with the best prospective outcome via feedback projections to the cortex. The cost-benefit model, while retaining the antagonistic roles of the two pathways for movements, requires co-activation of the two pathways during movement as both benefit and cost are computed for every movement. The cost-benefit model, though simple, accounts for a number of confounding results, and generates new focus for future research with testable predictions.

[1]  J. Wickens,et al.  Computational models of the basal ganglia: from robots to membranes , 2004, Trends in Neurosciences.

[2]  Y. Niv Cost, Benefit, Tonic, Phasic , 2007, Annals of the New York Academy of Sciences.

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

[4]  Stan B. Floresco,et al.  Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making , 2008, Cognitive, affective & behavioral neuroscience.

[5]  S. Schiffmann,et al.  D2R striatopallidal neurons inhibit both locomotor and drug reward processes , 2009, Nature Neuroscience.

[6]  R. Turner,et al.  Corticostriatal Activity in Primary Motor Cortex of the Macaque , 2000, The Journal of Neuroscience.

[7]  J. Penney,et al.  Differential loss of striatal projection neurons in Huntington disease. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

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

[9]  Ken-ichi Amemori,et al.  Localized Microstimulation of Primate Pregenual Cingulate Cortex Induces Negative Decision-Making , 2012, Nature Neuroscience.

[10]  M. Walton,et al.  Separate neural pathways process different decision costs , 2006, Nature Neuroscience.

[11]  Paul Greengard,et al.  Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors , 2010, Proceedings of the National Academy of Sciences.

[12]  J. Krakauer,et al.  Why Don't We Move Faster? Parkinson's Disease, Movement Vigor, and Implicit Motivation , 2007, The Journal of Neuroscience.

[13]  L. Vanderschuren,et al.  Critical Involvement of Dopaminergic Neurotransmission in Impulsive Decision Making , 2006, Biological Psychiatry.

[14]  F. Gonon,et al.  Cortical Inputs and GABA Interneurons Imbalance Projection Neurons in the Striatum of Parkinsonian Rats , 2006, The Journal of Neuroscience.

[15]  K. Deisseroth,et al.  Input-specific control of reward and aversion in the ventral tegmental area , 2012, Nature.

[16]  M. Platt,et al.  Risky business: the neuroeconomics of decision making under uncertainty , 2008, Nature Neuroscience.

[17]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[18]  G. E. Alexander,et al.  Parallel organization of functionally segregated circuits linking basal ganglia and cortex. , 1986, Annual review of neuroscience.

[19]  Kuei Yuan Tseng,et al.  Handbook of basal ganglia structure and function , 2010 .

[20]  L. Wilbrecht,et al.  Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action value , 2012, Nature Neuroscience.

[21]  P. Glimcher,et al.  Midbrain Dopamine Neurons Encode a Quantitative Reward Prediction Error Signal , 2005, Neuron.

[22]  C. Cepeda,et al.  Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[23]  G. G. Stokes "J." , 1890, The New Yale Book of Quotations.

[24]  M. Walton,et al.  Dissociable cost and benefit encoding of future rewards by mesolimbic dopamine , 2009, Nature Neuroscience.

[25]  A. Kacelnik,et al.  To walk or to fly? How birds choose among foraging modes. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[27]  Daryl M. Gohl,et al.  Layered reward signaling through octopamine and dopamine in Drosophila , 2012, Nature.

[28]  P. Greengard,et al.  Dichotomous Dopaminergic Control of Striatal Synaptic Plasticity , 2008, Science.

[29]  R. Rosenfeld Nature , 2009, Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery.

[30]  E. Richfield,et al.  Reduced expression of preproenkephalin in striatal neurons from huntington's disease patients , 1995, Annals of neurology.

[31]  D. Zald,et al.  Dopaminergic Mechanisms of Individual Differences in Human Effort-Based Decision-Making , 2012, The Journal of Neuroscience.

[32]  R. Shadmehr,et al.  Motor disorder in Huntington's disease begins as a dysfunction in error feedback control , 2000, Nature.

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

[34]  J. Salamone,et al.  Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits , 2007, Psychopharmacology.

[35]  G. Arbuthnott,et al.  Computational models of the basal ganglia , 2000, Movement disorders : official journal of the Movement Disorder Society.

[36]  C. Gerfen,et al.  D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. , 1990, Science.

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

[38]  Timothy Edward John Behrens,et al.  Effort-Based Cost–Benefit Valuation and the Human Brain , 2009, The Journal of Neuroscience.

[39]  Jeffrey R. Stevens,et al.  Will Travel for Food: Spatial Discounting in Two New World Monkeys , 2005, Current Biology.

[40]  O. Hikosaka,et al.  Two types of dopamine neuron distinctly convey positive and negative motivational signals , 2009, Nature.

[41]  A. Nambu Somatotopic Organization of the Primate Basal Ganglia , 2011, Front. Neuroanat..

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

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

[44]  S. Nakanishi,et al.  Distinct Roles of Synaptic Transmission in Direct and Indirect Striatal Pathways to Reward and Aversive Behavior , 2010, Neuron.

[45]  G. Friedlander [Signal]. , 2020, Medecine sciences : M/S.

[46]  A. Reiner,et al.  Evidence for Differential Cortical Input to Direct Pathway versus Indirect Pathway Striatal Projection Neurons in Rats , 2004, The Journal of Neuroscience.

[47]  R. Ivry,et al.  The coordination of movement: optimal feedback control and beyond , 2010, Trends in Cognitive Sciences.

[48]  Daniel M. Wolpert,et al.  Making smooth moves , 2022 .

[49]  E. Todorov Direct cortical control of muscle activation in voluntary arm movements: a model , 2000, Nature Neuroscience.

[50]  M. Frank Computational models of motivated action selection in corticostriatal circuits , 2011, Current Opinion in Neurobiology.

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

[52]  O. Hikosaka,et al.  Role of the basal ganglia in the control of purposive saccadic eye movements. , 2000, Physiological reviews.

[53]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

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