The Hierarchical Organisation of Cortical and Basal-Ganglia Systems: A Computationally-Informed Review and Integrated Hypothesis

To suitably adapt to the challenges posed by reproduction and survival, animals need to learn to select when to perform different behaviours, to have internal criteria for guiding these learning processes, and to perform behaviours efficiently once selected. To implement these processes, their brains must be organised in a suitable hierarchical fashion. Here we briefly review two types of neural/behavioural/computational literatures, focussed, respectively, on cortex and on sub-cortical areas, and highlight their important limitations. Then we review two computational modelling works of the authors that exemplify the problems, brain areas, experiments, main concepts, and limitations of the two research threads. Finally we propose a theoretical integration of the two views, showing how this allows us to solve most of the problems found by the two accounts if taken in isolation. The overall picture that emerges is that the cortical and the basal ganglia systems form two highly-organised hierarchical systems working in close synergy and jointly solving all the challenges of choice, selection, and implementation needed to acquire and express adaptive behaviour.

[1]  Michael I. Jordan,et al.  Optimal feedback control as a theory of motor coordination , 2002, Nature Neuroscience.

[2]  Benjamin O. Turner,et al.  Cortical and basal ganglia contributions to habit learning and automaticity , 2010, Trends in Cognitive Sciences.

[3]  John M. Ennis,et al.  A neurobiological theory of automaticity in perceptual categorization. , 2007, Psychological review.

[4]  Michael A. Arbib,et al.  Modeling parietal-premotor interactions in primate control of grasping , 1998, Neural Networks.

[5]  M. West,et al.  Changes in activity of the striatum during formation of a motor habit , 2007, The European journal of neuroscience.

[6]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

[7]  B. Balleine,et al.  Reward‐guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico‐basal ganglia networks , 2008, The European journal of neuroscience.

[8]  R. Ellis,et al.  The potentiation of grasp types during visual object categorization , 2001 .

[9]  M. Laubach,et al.  Dynamic Encoding of Action Selection by the Medial Striatum , 2009, The Journal of Neuroscience.

[10]  Alec Solway,et al.  Goal-directed decision making as probabilistic inference: a computational framework and potential neural correlates. , 2012, Psychological review.

[11]  T. Robbins,et al.  Putting a spin on the dorsal–ventral divide of the striatum , 2004, Trends in Neurosciences.

[12]  J. Deniau,et al.  Disinhibition as a basic process in the expression of striatal functions , 1990, Trends in Neurosciences.

[13]  Mitsuo Kawato,et al.  Internal models for motor control and trajectory planning , 1999, Current Opinion in Neurobiology.

[14]  Edward T. Bullmore,et al.  Modular and Hierarchically Modular Organization of Brain Networks , 2010, Front. Neurosci..

[15]  B. Balleine,et al.  The Role of the Nucleus Accumbens in Instrumental Conditioning: Evidence of a Functional Dissociation between Accumbens Core and Shell , 2001, The Journal of Neuroscience.

[16]  A. Keller,et al.  Long-term potentiation in the motor cortex. , 1989, Science.

[17]  K. Doya Complementary roles of basal ganglia and cerebellum in learning and motor control , 2000, Current Opinion in Neurobiology.

[18]  Tobias Bast,et al.  Toward an Integrative Perspective on Hippocampal Function: From the Rapid Encoding of Experience to Adaptive Behavior , 2007, Reviews in the neurosciences.

[19]  Claudio Galletti,et al.  Functional imaging of the parietal cortex during action execution and observation. , 2009, Cerebral cortex.

[20]  Michael A. Arbib,et al.  Schema design and implementation of the grasp-related mirror neuron system , 2002, Biological Cybernetics.

[21]  Graeme D. Ruxton,et al.  Modelling Perception with Artificial Neural Networks: General themes , 2010 .

[22]  T. Prescott,et al.  The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. , 2010, Progress in Neurobiology.

[23]  T. Ziemke,et al.  Theories and computational models of affordance and mirror systems: An integrative review , 2013, Neuroscience & Biobehavioral Reviews.

[24]  Nikolaus R. McFarland,et al.  Striatonigrostriatal Pathways in Primates Form an Ascending Spiral from the Shell to the Dorsolateral Striatum , 2000, The Journal of Neuroscience.

[25]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[26]  E. Miller,et al.  An integrative theory of prefrontal cortex function. , 2001, Annual review of neuroscience.

[27]  M. Bear,et al.  Experience-dependent modification of synaptic plasticity in visual cortex , 1996, Nature.

[28]  J. Lisman,et al.  The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory , 2005, Neuron.

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

[30]  Marco Mirolli,et al.  Phasic dopamine as a prediction error of intrinsic and extrinsic reinforcements driving both action acquisition and reward maximization: A simulated robotic study , 2013, Neural Networks.

[31]  E. Rolls,et al.  Neural networks and brain function , 1998 .

[32]  Joel L. Davis,et al.  Adaptive Critics and the Basal Ganglia , 1995 .

[33]  D. Pandya,et al.  Corticostriatal connections of extrastriate visual areas in rhesus monkeys. , 1995, The Journal of comparative neurology.

[34]  J. Rothwell,et al.  Short latency inhibition of human hand motor cortex by somatosensory input from the hand , 2000, The Journal of physiology.

[35]  Masao Ito Control of mental activities by internal models in the cerebellum , 2008, Nature Reviews Neuroscience.

[36]  James M. Kilner,et al.  More than one pathway to action understanding , 2011, Trends in Cognitive Sciences.

[37]  Alan Cowey,et al.  Transcranial magnetic stimulation and cognitive neuroscience , 2000, Nature Reviews Neuroscience.

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

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

[40]  M. West,et al.  Loss of Lever Press-Related Firing of Rat Striatal Forelimb Neurons after Repeated Sessions in a Lever Pressing Task , 1997, The Journal of Neuroscience.

[41]  J. Fuster The Prefrontal Cortex—An Update Time Is of the Essence , 2001, Neuron.

[42]  G. Rizzolatti,et al.  Premotor cortex and the recognition of motor actions. , 1996, Brain research. Cognitive brain research.

[43]  M. Graziano,et al.  New Insights into Motor Cortex , 2011, Neuron.

[44]  Domenico Parisi,et al.  A NEURAL-NETWORK MODEL OF THE DYNAMICS OF HUNGER, LEARNING, AND ACTION VIGOR IN MICE , 2009 .

[45]  B. Bernstein,et al.  Animal Behavior , 1927, Japanese Marine Life.

[46]  L. Barsalou Grounded cognition. , 2008, Annual review of psychology.

[47]  P. Dayan,et al.  Uncertainty-based competition between prefrontal and dorsolateral striatal systems for behavioral control , 2005, Nature Neuroscience.

[49]  K. Berridge,et al.  What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? , 1998, Brain Research Reviews.

[50]  A. Cangelosi,et al.  How affordances associated with a distractor object affect compatibility effects: A study with the computational model TRoPICALS , 2013, Psychological research.

[51]  Frank Telang,et al.  Depressed dopamine activity in caudate and preliminary evidence of limbic involvement in adults with attention-deficit/hyperactivity disorder. , 2007, Archives of general psychiatry.

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

[53]  Paul Cisek,et al.  Cortical mechanisms of action selection: the affordance competition hypothesis , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  Nuttapong Chentanez,et al.  Intrinsically Motivated Learning of Hierarchical Collections of Skills , 2004 .

[55]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[56]  S P Wise,et al.  Distributed modular architectures linking basal ganglia, cerebellum, and cerebral cortex: their role in planning and controlling action. , 1995, Cerebral cortex.

[57]  Joseph E LeDoux,et al.  Organization of intra-amygdaloid circuitries in the rat: an emerging framework for understanding functions of the amygdala , 1997, Trends in Neurosciences.

[58]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[59]  Frank E. Pollick,et al.  Neural Substrates for Action Understanding at Different Description Levels in the Human Brain , 2008, Journal of Cognitive Neuroscience.

[60]  G. Heit,et al.  Somatotopy in the basal ganglia: experimental and clinical evidence for segregated sensorimotor channels , 2005, Brain Research Reviews.

[61]  Rob Ellis,et al.  Does selecting one visual object from several require inhibition of the actions associated with nonselected objects? , 2007, Journal of experimental psychology. Human perception and performance.

[62]  Francesco Mannella,et al.  A system-level neural model of the brain mechanisms underlying instrumental devaluation in rats , 2011 .

[63]  B. Balleine,et al.  Goal-directed instrumental action: contingency and incentive learning and their cortical substrates , 1998, Neuropharmacology.

[64]  Peter Redgrave,et al.  A computational model of action selection in the basal ganglia. I. A new functional anatomy , 2001, Biological Cybernetics.

[65]  D. Parisi,et al.  TRoPICALS: a computational embodied neuroscience model of compatibility effects. , 2010, Psychological review.

[66]  Francesco Mannella,et al.  The roles of the amygdala in the affective regulation of body, brain, and behaviour , 2010, Connect. Sci..

[67]  Afdc Hamilton,et al.  The motor hierarchy: from kinematics to goals and intentions , 2007 .

[68]  A. Grace,et al.  Regulation of firing of dopaminergic neurons and control of goal-directed behaviors , 2007, Trends in Neurosciences.

[69]  P. Strick,et al.  Basal ganglia and cerebellar loops: motor and cognitive circuits , 2000, Brain Research Reviews.

[70]  L. Heimer,et al.  Ventral striatum and ventral pallidum Components of the motor system? , 1982, Trends in Neurosciences.

[71]  R. Mansfield,et al.  Analysis of visual behavior , 1982 .

[72]  H. Asanuma,et al.  Projection from the sensory to the motor cortex is important in learning motor skills in the monkey. , 1993, Journal of neurophysiology.

[73]  H. Bergman,et al.  Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease , 2010, Nature Reviews Neuroscience.

[74]  Seth A. Herd,et al.  A Unified Framework for Inhibitory Control Opinion , 2022 .

[75]  G. Baldassarre,et al.  Modelling Perception with Artificial Neural Networks: The interplay of Pavlovian and instrumental processes in devaluation experiments: a computational embodied neuroscience model tested with a simulated rat , 2010 .

[76]  M. Jeannerod Visuomotor channels: Their integration in goal-directed prehension , 1999 .

[77]  Teuvo Kohonen Self–organized maps of sensory events , 2003, Philosophical Transactions of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[78]  G. Rizzolatti,et al.  The mirror-neuron system. , 2004, Annual review of neuroscience.

[79]  K. C. Anderson,et al.  Single neurons in prefrontal cortex encode abstract rules , 2001, Nature.

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

[81]  Peter Dayan,et al.  Theoretical Neuroscience: Computational and Mathematical Modeling of Neural Systems , 2001 .

[82]  E. Abercrombie,et al.  Differential Effect of Stress on In Vivo Dopamine Release in Striatum, Nucleus Accumbens, and Medial Frontal Cortex , 1989, Journal of neurochemistry.

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

[84]  Eytan Ruppin,et al.  Actor-critic models of the basal ganglia: new anatomical and computational perspectives , 2002, Neural Networks.

[85]  A. Dickinson,et al.  Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour , 2001, The European journal of neuroscience.

[86]  M. Botvinick,et al.  Hierarchically organized behavior and its neural foundations: A reinforcement learning perspective , 2009, Cognition.

[87]  Edward F. Jackson,et al.  Caudate Nucleus Volume Asymmetry Predicts Attention-Deficit Hyperactivity Disorder (ADHD) Symptomatology in Children , 2002, Journal of child neurology.

[88]  E. Rolls,et al.  Attention and working memory: a dynamical model of neuronal activity in the prefrontal cortex , 2003, The European journal of neuroscience.

[89]  J. Houk,et al.  Cerebellar guidance of premotor network development and sensorimotor learning. , 1997, Learning & memory.

[90]  P. Goldman-Rakic,et al.  Differential Activation of the Caudate Nucleus in Primates Performing Spatial and Nonspatial Working Memory Tasks , 1997, The Journal of Neuroscience.

[91]  T. Robbins,et al.  Striatal contributions to working memory: a functional magnetic resonance imaging study in humans , 2004, The European journal of neuroscience.

[92]  G. Rizzolatti,et al.  Parietal Lobe: From Action Organization to Intention Understanding , 2005, Science.

[93]  D. S. Zahm,et al.  An integrative neuroanatomical perspective on some subcortical substrates of adaptive responding with emphasis on the nucleus accumbens , 2000, Neuroscience & Biobehavioral Reviews.

[94]  G. Schöner,et al.  Dynamic Field Theory of Movement Preparation , 2022 .

[95]  B. Balleine,et al.  The General and Outcome-Specific Forms of Pavlovian-Instrumental Transfer Are Differentially Mediated by the Nucleus Accumbens Core and Shell , 2011, The Journal of Neuroscience.

[96]  P. Strick,et al.  The temporal lobe is a target of output from the basal ganglia. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[97]  B. Everitt,et al.  Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex , 2002, Neuroscience & Biobehavioral Reviews.

[98]  C. Summerfield,et al.  An information theoretical approach to prefrontal executive function , 2007, Trends in Cognitive Sciences.

[99]  A. Graybiel,et al.  Adaptive neural networks in the basal ganglia. , 1995 .

[100]  S. Haber The primate basal ganglia: parallel and integrative networks , 2003, Journal of Chemical Neuroanatomy.

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

[102]  Colin Wilson The contribution of cortical neurons to the firing pattern of striatal spiny neurons , 1995 .

[103]  J. Kalaska,et al.  Neural mechanisms for interacting with a world full of action choices. , 2010, Annual review of neuroscience.