Skip to main content

Basal Ganglia System as an Engine for Exploration

  • Living reference work entry
  • First Online:

Definition

The basal ganglia (BG) system is a deep brain circuit with wide-ranging brain functions. Exploration refers to the sampling of a variety of behaviors not firmly established within a learned repertoire. While the neural source of variability driving exploration within the subcortex has not been identified, the hypothesis that the indirect pathway of the BG is the subcortical substrate for exploration leads to explanations for how a range of putative BG functions might be performed.

Detailed Description

Reinforcement Learning and the Basal Ganglia

For nearly a century, a certain “mysteriousness” has been attributed to the function of the basal ganglia (BG) system – a deep brain circuit of multiple interconnected nuclei, with rich connections to large parts of the cortex (Kinnier Wilson in his Croonian lectures in 1925, Marsden 1982). The mystique surrounding BG has its roots perhaps in the multifarious functions of this circuit. Action selection, action gating, sequence...

This is a preview of subscription content, log in via an institution.

References

  • Albin RL, Young AB et al (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12(10):366–375

    Article  CAS  PubMed  Google Scholar 

  • Alexander GE, Crutcher MD (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13(7):266–271

    Article  CAS  PubMed  Google Scholar 

  • Baunez C, Humby T et al (2001) Effects of STN lesions on simple vs choice reaction time tasks in the rat: preserved motor readiness, but impaired response selection. Eur J Neurosci 13(8):1609–1616

    Article  CAS  PubMed  Google Scholar 

  • Bergman H, Wichmann T et al (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72(2):507–520

    CAS  PubMed  Google Scholar 

  • Brown P, Oliviero A et al (2001) Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson’s disease. J Neurosci 21(3):1033–1038

    CAS  PubMed  Google Scholar 

  • Brunel N (2000) Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons. J Comput Neurosci 8(3):183–208

    Article  CAS  PubMed  Google Scholar 

  • Chakravarthy VS (2013) Do basal ganglia amplify willed action by stochastic resonance? A model. PLoS One 8(11):e75657

    Article  PubMed Central  PubMed  Google Scholar 

  • Chakravarthy VS, Joseph D et al (2010) What do the basal ganglia do? A modeling perspective. Biol Cybern 103(3):237–253

    Article  CAS  PubMed  Google Scholar 

  • Contreras-Vidal J, Stelmach GE (1995) Effects of Parkinsonism on motor control. Life Sci 58(3):165–176

    Article  CAS  Google Scholar 

  • Cowie D, Limousin P et al (2010) Insights into the neural control of locomotion from walking through doorways in Parkinson’s disease. Neuropsychologia 48(9):2750–2757

    Article  PubMed  Google Scholar 

  • Daw ND, O’Doherty JP et al (2006) Cortical substrates for exploratory decisions in humans. Nature 441(7095):876–879

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13(7):281–285

    Article  CAS  PubMed  Google Scholar 

  • Devan BD, White NM (1999) Parallel information processing in the dorsal striatum: relation to hippocampal function. J Neurosci 19(7):2789–2798

    CAS  PubMed  Google Scholar 

  • Doya K (2002) Metalearning and neuromodulation. Neural Netw 15(4–6):495–506

    Article  PubMed  Google Scholar 

  • Gillies A, Willshaw D et al (2002) Functional interactions within the subthalamic nucleus. The basal ganglia VII. Springer, New York. pp 359–368

    Google Scholar 

  • Grabli D, McCairn K et al (2004) Behavioural disorders induced by external globus pallidus dysfunction in primates: I. Behavioural study. Brain 127(9):2039–2054

    Article  PubMed  Google Scholar 

  • Gupta A, Balasubramani PP et al (2013) Computational model of precision grip in Parkinson’s disease: a utility based approach. Front Comput Neurosci 7:172

    Article  PubMed Central  PubMed  Google Scholar 

  • Gurney K, Prescott TJ et al (2001) A computational model of action selection in the basal ganglia. I. A new functional anatomy. Biol Cybern 84(6):401–410

    Article  CAS  PubMed  Google Scholar 

  • Hollerman JR, Schultz W (1998) Dopamine neurons report an error in the temporal prediction of reward during learning. Nat Neurosci 1(4):304–309

    Article  CAS  PubMed  Google Scholar 

  • Houk JC, Davis JL et al (1995) Models of information processing in the basal ganglia. The MIT press, Cambridge, MA

    Google Scholar 

  • Humphries M, Gurney K (2002) The role of intra-thalamic and thalamocortical circuits in action selection. Netw Comput Neural Syst 13(1):131–156

    Article  CAS  Google Scholar 

  • Humphries MD, Prescott TJ (2010) The ventral basal ganglia, a selection mechanism at the crossroads of space, strategy, and reward. Prog Neurobiol 90(4):385–417

    Article  PubMed  Google Scholar 

  • Hurtado JM, Gray CM et al (1999) Dynamics of tremor-related oscillations in the human globus pallidus: a single case study. Proc Natl Acad Sci 96(4):1674–1679

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Joel D, Niv Y et al (2002) Actor-critic models of the basal ganglia: new anatomical and computational perspectives. Neural Netw 15(4–6):535–547

    Article  PubMed  Google Scholar 

  • Kalva SK, Rengaswamy M et al (2012) On the neural substrates for exploratory dynamics in basal ganglia: a model. Neural Netw 32:65–73

    Article  PubMed  Google Scholar 

  • Kirkpatrick S, Gelatt CD Jr et al (1983) Optimization by simulated annealing. Science 220(4598):671–680

    Article  CAS  PubMed  Google Scholar 

  • Kliem MA, Maidment NT et al (2007) Activation of nigral and pallidal dopamine D1-like receptors modulates basal ganglia outflow in monkeys. J Neurophysiol 98(3):1489–1500

    Article  CAS  PubMed  Google Scholar 

  • Knutson B, Adams CM et al (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21(16):RC159

    CAS  PubMed  Google Scholar 

  • Kravitz AV, Freeze BS et al (2010) Regulation of Parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466(7306):622–626

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Krishnan R, Ratnadurai S et al (2011) Modeling the role of basal ganglia in saccade generation: is the indirect pathway the explorer? Neural Netw 24(8):801–813

    Article  CAS  PubMed  Google Scholar 

  • Magdoom KN, Subramanian D et al (2011) Modeling basal ganglia for understanding Parkinsonian reaching movements. Neural Comput 23(2):477–516

    Article  CAS  PubMed  Google Scholar 

  • Magill P, Bolam J et al (2001) Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus–globus pallidus network. Neuroscience 106(2):313–330

    Article  CAS  PubMed  Google Scholar 

  • Marsden C (1982) The mysterious motor function of the basal ganglia: the Robert Wartenberg lecture. Neurology 32:514–539

    Article  CAS  PubMed  Google Scholar 

  • Mink JW (2003) The basal ganglia and involuntary movements: impaired inhibition of competing motor patterns. Arc Neurol 60(10):1365

    Article  Google Scholar 

  • Miyoshi E, Wietzikoski S et al (2002) Impaired learning in a spatial working memory version and in a cued version of the water maze in rats with MPTP-induced mesencephalic dopaminergic lesions. Brain Res Bull 58(1):41–47

    Article  CAS  PubMed  Google Scholar 

  • Muralidharan V, Balasubramani PP et al (2013) A computational model of altered gait patterns in parkinson’s disease patients negotiating narrow doorways. Front Comput Neurosci 7:190

    PubMed Central  Google Scholar 

  • O’Doherty J, Dayan P et al (2004) Dissociable roles of ventral and dorsal striatum in instrumental conditioning. Science 304(5669):452–454

    Article  PubMed  Google Scholar 

  • Plenz D, Kital ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400(6745):677–682

    Article  CAS  PubMed  Google Scholar 

  • Priyadharsini BP, Ravindran B et al (2012) Understanding the role of serotonin in basal ganglia through a unified model. Artificial neural networks and machine learning–ICANN 2012, Springer, Berlin, pp 467–473

    Google Scholar 

  • Redgrave P, Prescott TJ et al (1999) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience 89(4):1009–1023

    Article  CAS  PubMed  Google Scholar 

  • Ring H, Serra-Mestres J (2002) Neuropsychiatry of the basal ganglia. J Neurol Neurosurg Psychiatry 72(1):12–21

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Rushworth MF, Behrens TE (2008) Choice, uncertainty and value in prefrontal and cingulate cortex. Nat Neurosci 11(4):389–397

    Article  CAS  PubMed  Google Scholar 

  • Russell V, Allin R et al (1992) Regional distribution of monoamines and dopamine D1-and D2-receptors in the striatum of the rat. Neurochem Res 17(4):387–395

    Article  CAS  PubMed  Google Scholar 

  • Schultz W, Dayan P et al (1997) A neural substrate of prediction and reward. Science 275(5306):1593–1599

    Article  CAS  PubMed  Google Scholar 

  • Sridharan D, Prashanth PS et al (2006) The role of the basal ganglia in exploration in a neural model based on reinforcement learning. Int J Neural Syst 16(2):111–124

    Article  CAS  PubMed  Google Scholar 

  • Stein PS, Grillner S et al (1997) Neurons, networks, and behavior. MIT Press, Cambridge, MA

    Google Scholar 

  • Steiner H, Tseng KY (2010) Handbook of basal ganglia structure and function: a decade of progress. Access online via Elsevier. Academic press, San Diego

    Google Scholar 

  • Sukumar D, Rengaswamy M et al (2012) Modeling the contributions of basal ganglia and hippocampus to spatial navigation using reinforcement learning. PLoS One 7(10):e47467

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sutton R, Barto A (1998) Reinforcement learning: an introduction. Adaptive computations and machine learning. MIT Press/Bradford, Cambridge, MA

    Google Scholar 

  • Terman D, Rubin J et al (2002) Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J Neurosci 22(7):2963–2976

    CAS  PubMed  Google Scholar 

  • Usher M, Cohen JD et al (1999) The role of locus coeruleus in the regulation of cognitive performance. Science 283(5401):549–554

    Article  CAS  PubMed  Google Scholar 

  • Willshaw D, Li Z (2002) Subthalamic–pallidal interactions are critical in determining normal and abnormal functioning of the basal ganglia. Proc R Soc Lond Ser B Biol Sci 269(1491):545–551

    Article  Google Scholar 

  • Yoshida W, Ishii S (2006) Resolution of uncertainty in prefrontal cortex. Neuron 50(5):781–789

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. Srinivasa Chakravarthy .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this entry

Cite this entry

Chakravarthy, V.S., Balasubramani, P.P. (2014). Basal Ganglia System as an Engine for Exploration. In: Jaeger, D., Jung, R. (eds) Encyclopedia of Computational Neuroscience. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-7320-6_81-1

Download citation

  • DOI: https://doi.org/10.1007/978-1-4614-7320-6_81-1

  • Received:

  • Accepted:

  • Published:

  • Publisher Name: Springer, New York, NY

  • Online ISBN: 978-1-4614-7320-6

  • eBook Packages: Springer Reference Biomedicine and Life SciencesReference Module Biomedical and Life Sciences

Publish with us

Policies and ethics