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10 - Action selection and refinement in subcortical loops through basal ganglia and cerebellum

from Part II - Computational neuroscience models

Published online by Cambridge University Press:  05 November 2011

Anil K. Seth
Affiliation:
University of Sussex
Tony J. Prescott
Affiliation:
University of Sheffield
Joanna J. Bryson
Affiliation:
University of Bath
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Summary

Summary

Subcortical loops through the basal ganglia and cerebellum form computationally powerful distributed processing modules (DPMs). This chapter relates the computational features of a DPM's loop through the basal ganglia to experimental results for two kinds of natural action selection. First, data from both monkeys and humans in a step-tracking task were used to decipher the neural mechanisms that underlie the detection of movement errors leading to selection of corrective movements called submovements. Second, functional brain imaging of human subjects during a serial-order recall task was used to study brain activity associated with decoding a sequence of actions from information held in working memory. Our DPM-based model assists in the interpretation of puzzling data from both of these experiments. These analyses lead to a broad discussion of the DPM concept and how it relates to neuroscience, modularity, engineering, evolution, mathematical recursion, agent-based modelling, Bayesian computations, and brain disorders. The loops through basal ganglia and cerebellum profit from exceptional combinations of unique cellular properties together with advantageous neural circuitry. Their modular organisation means that DPMs regulate pattern formation in multiple areas of the cerebral cortex, thus initiating and refining different kinds of action (or thought), depending on the area of the brain. We then use our findings to formulate a novel model of the etiology of schizophrenia.

Introduction

The higher order circuitry of the brain is comprised of a large-scale network of distributed processing modules (DPMs). Each of approximately 100 cerebral cortical areas is individually regulated by relatively private loops through subcortical structures, particularly through the basal ganglia and cerebellum (Houk, 2005; Houk and Wise, 1995; Kelly and Strick, 2003, 2004). These DPMs have powerful computational architectures as summarised in Figure 10.1. Each DPM receives cortico-cortical input vectors from approximately seven other DPMs (although only two are shown in Figure 10.1). (The estimate of seven derives from Felleman and Van Essen, 1991.) The final outcome of all of the computations in a given DPM is a spatiotemporal pattern of activity in the module's output vector, representing the activity in its set of cortical output neurons. This output is sent as input to other DPMs, or to the brainstem or spinal cord. In this manner, arrays of DPMs form large-scale networks that function in combination to control behaviour, or thought. The reader should consult Houk (2005) for a detailed description of this architecture and a justification of its capacity to control both actions and thoughts. The brief overview of functional operations in loops through basal ganglia (BG) and cerebellum (CB) given in the next two paragraphs is a summary that applies to the selection and initiation of movement commands that control discrete actions.

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Publisher: Cambridge University Press
Print publication year: 2011

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References

Andreasen, N.C 1999 A unitary model of schizophrenia: Bleuler's ‘fragmented phrene’ as schizencephalyArch. Gen. Psychiatry 56 781CrossRefGoogle ScholarPubMed
Arbib, M. AA. Billard, M. IacoboniOztop, E 2000 Synthetic brain imaging: grasping, mirror neurons and imitationNeural. Netw 13 975CrossRefGoogle ScholarPubMed
Barringer, CBarto, A. GHouk, J. C 2008 Simulated reaching supports the Normalized Predicted Error (NPE) discrete control hypothesis for on-line error correction of voluntary movementsSociety for Neuroscience 2008 Washington DCGoogle Scholar
Barto, A.GFagg, A. HSitkoff, NHouk, J. C 1999 A cerebellar model of timing and prediction in the control of reachingNeural Comput 11 565CrossRefGoogle ScholarPubMed
Beiser, D. GHouk, J. C 1998 Model of cortical-basal ganglionic processing: encoding the serial order of sensory eventsJ. Neurophysiol 79 3168CrossRefGoogle ScholarPubMed
Berlim, M. TMattevi, B. SBelmonte-de-Abreu, PCrow, T. J 2003 The etiology of schizophrenia and the origin of language: Overview of a theoryCompr. Psychiat 44 7CrossRefGoogle ScholarPubMed
Berthier, N. ESingh, S. PBarto, A. GHouk, J. C 1993 Distributed representation of limb motor programs in arrays of adjustable pattern generators. Cogn. Neurosci 5 56CrossRefGoogle ScholarPubMed
Bhushan, NShadmehr, R 1999 Evidence for a forward dynamics model in human adaptive motor controlIn Advances in Neural Processing SystemsKearns, M. SSolla, S. ACohn, D. ACambridge, MAMIT Press, pp. 3–9Google Scholar
Bliss, T. V. PCollingridge, G. L 1993 A synaptic model of memory: long-term potentiation in the hippocampusNature 361 31CrossRefGoogle ScholarPubMed
Booth, J. RWood, LLu, DHouk, J. CBitan, T 2007 The role of the basal ganglia and cerebellum in language processingBrain Res 1133 136CrossRefGoogle ScholarPubMed
Borrell, JVela, J. MArevalo-Martin, AMolina-Holgado, EGuaza, C 2002 Prenatal immune challenge disrupts sensorimotor gating in adult rats. Implications for the etiopathogenesis of schizophreniaNeuropsychopharmacology 26 204CrossRefGoogle ScholarPubMed
Botvinick, M. MPlaut, D. C 2006 Short-term memory for serial order: a recurrent neural network modelPsychol. Rev 113 201CrossRefGoogle ScholarPubMed
Botvinick, M. MWang, JCowan, E 2009 An analysis of immediate serial recall performance in a MacaqueAnim. Cogn. doi 10 s10071Google Scholar
Bowery, N. GHudson, A. LPrice, G. W 1987 GABAA and GABAB receptor site distribution in the rat central nervous systemNeuroscience 20 365CrossRefGoogle ScholarPubMed
Bowery, N. GParry, KGoodrich, GIllinsky, IKultas-Illinsky, K 1999 Distribution of GABA(B) binding sites in the thalamus and basal ganglia of the rhesus monkey ()Neuropharmacology 38 1675CrossRefGoogle Scholar
Brasted, P. JWise, S. P 2004 Comparison of learning-related neuronal activity in the dorsal premotor cortex and striatumEur. J. Neurosci 19 721CrossRefGoogle ScholarPubMed
Breese, C. RAdams, CLogel, J 1997 Comparison of the regional expression of nicotinic acetylcholine receptor α7 mRNA and [125I]-α-Bungarotoxzin binding in human postmortem brainJ. Comp. Neurol 387 3853.0.CO;2-X>CrossRefGoogle ScholarPubMed
Calabresi, PMercuri, N. BDeMurtas, MBernardi, G 1991 Involvement of GABA systems in feedback regulation of glutamate- and GABA-mediated synaptic potentials in rat neostriatumJ. Physiol 440 581CrossRefGoogle ScholarPubMed
Carelli, R. MWolske, MWest, M. O 1997 Loss of lever press-related firing of rat striatal forelimb neurons after repeated sessions in a lever pressing taskJ. Neurosci 17 1804CrossRefGoogle Scholar
Crow, T. J 1997 Is schizophrenia the price that pays for language?Schizophr. Res 28 127CrossRefGoogle ScholarPubMed
Doya, K 1999 What are the computations of the cerebellum, the basal ganglia and the cerebral cortex?Neural Networks 12 961CrossRefGoogle ScholarPubMed
Elman, J. L 2004 An alternative view of the mental lexiconTrends Cogn. Sci 8 301CrossRefGoogle ScholarPubMed
Enna, S. JBowery, N. G 2004 GABAb receptor alterations as indicators of physiological and pharmacological functionBiochem. Pharma 68 1541CrossRefGoogle Scholar
Felleman, D. JVan Essen, D. C 1991 Distributed hierarchical processing in the primate cerebral cortexCereb. Cortex 1 1CrossRefGoogle ScholarPubMed
Fishbach, ARoy, S. ABastianen, CMiller, L. EHouk, J. C 2005 Kinematic properties of on-line error corrections in the monkeyExp. Br. Res 164 442CrossRefGoogle ScholarPubMed
Fishbach, ARoy, S. ABastianen, CMiller, L. EHouk, J. C 2007 Deciding when and how to correct a movement: discrete submovements as a decision making processExp. Br. Res 177 45CrossRefGoogle ScholarPubMed
Frank, M. J 2005 Dynamic dopamine modulation in the basal ganglia: a neurocomputational account of cognitive deficits in medicated and nonmedicated ParkinsonismJ. Cogn. Neurosci 17 51CrossRefGoogle ScholarPubMed
Fraser, DPark, SClark, GYohanna, DHouk, J. C 2004 Spatial serial order processing in schizophreniaSchizophr. Res 70 203CrossRefGoogle Scholar
Fraser, DReber, PParrish, TCortical neural correlates of serial order recall: cognitive and motor decodingSociety for Neuroscience 38th Annual Meeting 2008 28Google Scholar
Freedman, RLeonard, SOliney, A 2001 Evidence for the multigenic inheritance of schizophreniaAm. J. Med. Gen 105 794CrossRefGoogle ScholarPubMed
Freeman, W. J 2000 Mesoscopic neurodynamics: from neuron to brainJ. Physiol. Paris 94 303CrossRefGoogle Scholar
Gdowski, M. J, L. EMiller, CBastianen, E. K. NenoneneHouk, J. C 2007 Signaling patterns of globus pallidus internal segment neurons during forearm rotationBrain Res 1155 56CrossRefGoogle ScholarPubMed
Georgopoulos, A. P 1995 Motor cortex and cognitive processingThe Cognitive NeurosciencesGazzaniga, M. SCambridge, MAMIT Press507Google Scholar
Gibson, A. RHouk, J. CKohlerman, N. J 1985 Relation between red nucleus discharge and movement parameters in trained macaque monkeysJ. Physiol. (Lond.) 358 551CrossRefGoogle ScholarPubMed
Gruber, A. JSolla, S. ASurmeier, D. JHouk, J. C 2003 Modulation of striatal single units by expected reward: a spiny neuron model displaying dopamine-induced bistabilityJ. Neurophys 90 1095CrossRefGoogle ScholarPubMed
Gurney, KPrescott, T. JRedgrave, P 2001 A computational model of action selection in the basal ganglia. I. A new functional anatomyBiol. Cybern 84 401CrossRefGoogle ScholarPubMed
Gusnard, D. ARaichle, M. E 2001 Searching for a baseline: functional imaging and the resting human brainNature Rev. Neurosci 2 685CrossRefGoogle ScholarPubMed
Hauser, M. DChomsky, NFitch, W. T 2002 The faculty of language: what it is, who has it, and how did it evolveScience 298 1569CrossRefGoogle ScholarPubMed
Holdefer, R. NHouk, J. CMiller, L. E 2005 Movement-related discharge in the cerebellar nuclei persists after local injections of GABA-A antagonistsJ. Neurophysiol 93 35CrossRefGoogle ScholarPubMed
Houk, J. C 2001 Neurophysiology of frontal-subcortical loopsFrontal-Subcortical Circuits in Psychiatry and NeurologyLichter, D. GCummings, J. LNew YorkGuilford Publications92Google Scholar
Houk, J. C 2005 Agents of the mindBiol. Cybern 92 427CrossRefGoogle ScholarPubMed
Houk, J. C 2007 22663http://www.scholarpedia.org/article/Models_of_Basal_Ganglia
Houk, J. C 2010 Voluntary movement: control, learning and memoryEncyclopedia of Behavioral NeuroscienceKoob, G. FLe Moal, MThompson, R. FOxfordAcademic Press455CrossRefGoogle Scholar
Houk, J. C.Adams, J. LBarto, A. G 1995 A model of how the basal ganglia generates and uses neural signals that predict reinforcementModels of Information Processing in the Basal GangliaHouk, J. CDavis, J. LBeiser, D. GCambridge, MAMIT Press249Google Scholar
Houk, J. CBastianen, CFansler, D 2007 Action selection in subcortical loops through the basal ganglia and cerebellumPhil. Trans. R. Soc. B 362 1573CrossRefGoogle ScholarPubMed
Houk, J. CFagg, A. HBarto, A. G 2002 Fractional power damping model of joint motionProgress in Motor Control: Structure–Function Relations in Voluntary MovementsWrisberg, C. ALatash, MChampaign, ILHuman Kinetics147Google Scholar
Houk, J. CKeifer, JBarto, A. G 1993 Distributed motor commands in the limb premotor networkTrends Neurosci 16 27CrossRefGoogle ScholarPubMed
Houk, J. CMugnaini, E 2003 CerebellumFundamental NeuroscienceSquire, L. ROxfordAcademic Press841Google Scholar
Houk, J. CMugnaini, ERedei, E 2009 17652
Houk, J. CWise, S. P 1995 Distributed modular architectures linking basal ganglia, cerebellum, and cerebral cortex: their role in planning and controlling actionCerebral Cortex 5 95CrossRefGoogle ScholarPubMed
Hua, S. EHouk, J. C 1997 Cerebellar guidance of premotor network development and sensorimotor learningLearn. Mem 4 63CrossRefGoogle ScholarPubMed
Huxley, JMayr, EOsmond, HHoffer, A 1964 Schizophrenia as a genetic morphismNature 204 220CrossRefGoogle ScholarPubMed
Karniel, AInbar, G. F 1999 The use of a nonlinear muscle model in explaining the relationship between duration, amplitude, and peak velocity of human rapid movementsJ. Motor Behav 31 203CrossRefGoogle ScholarPubMed
Kawato, MKatayama, MGomi, HKoike, Y 1992 Coordinated arm movements: Virtual trajectory control hypothesis and learning inverse modelsInternational Symposium on Information SciencesIizuka KyusyuuJapanGoogle Scholar
Kelly, R. MStrick, P. L 2003 Cerebellar loops with motor cortex and prefrontal cortex of a nonhuman primateJ. Neurosci 23 8432CrossRefGoogle ScholarPubMed
Kelly, R. MStrick, P. L 2004 Macro-architecture of basal ganglia loops with the cerebral cortex: use of rabies virus to reveal multisynaptic circuitsProg. Brain Res 143 449Google ScholarPubMed
Kincaid, A. EZheng, TWilson, C. J 1998 Connectivity and convergence of single corticostriatal axonsJ. Neurosci 18 4722CrossRefGoogle ScholarPubMed
Koerding, K 2007 Decision theory: what ‘should’ the nervous system do?Science 318 606CrossRefGoogle Scholar
Kuttner, R. ELorincz, A. BSwan, D. A 1967 The schizophrenia gene and social evolutionPsychol. Rep 20 407CrossRefGoogle ScholarPubMed
Lacey, C. JBoyes, JGerlach, O 2005 GABAb receptors at glutamatergic synapses in the rat striatumNeuroscience 136 1083CrossRefGoogle Scholar
Lashley, K. S 1951 The problem of serial order in behaviorCerebral Mechanisms in BehaviorJeffres, L. ANew YorkJohn Wiley and Sons, Inc., pp.112Google Scholar
Lein, E. SHawrylycz, M. JAo, N 2006 Genome-wide atlas of gene expression in the adult mouse brainNature 445 168CrossRefGoogle ScholarPubMed
Logothetis, N 2002 The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signalPhil. Trans. R. Soc. Lond. B 357 1003CrossRefGoogle ScholarPubMed
Lu, XHikosaka, OMiyachi, S 1998 Role of monkey cerebellar nuclei in skill for sequential movementJ. Neurophysiol 79 2245CrossRefGoogle ScholarPubMed
Martin, S. CRussek, S. JFarb, D. H 2001 Human GABAbR genomic structure: evidence for splice variants in GABAbR1 but not GABAbR2Gene 278 63CrossRefGoogle Scholar
Matsuzaka, YPicard, NStrick, P. L 2007 Skill representation in the primary motor cortex after long-term practiceJ. Neurophysiol 97 1819CrossRefGoogle ScholarPubMed
Matthysse, SHolzman, P. SGusella, J. F 2004 Linkage of eye movement dysfunction to chromosome 6p in schizophrenia: additional evidenceAm. J. Med. Genet. B Neuropsychiatr. Genet 128 30CrossRefGoogle Scholar
Merzenich, MWright, BJenkins, W 1996 Cortical plasticity underlying perceptual, motor, and cognitive skill development: implications for neurorehabilitationCold Spring Harb. Symp. Quant. Biol 61 1Google ScholarPubMed
Miller, G. A 1956 The magical number seven, plus or minus two: some limits to our capacity for processing informationJ. Exp. Psychol 41 329CrossRefGoogle Scholar
Newman, P. PReza, H 1979 Functional relationships between the hippocampus and the cerebellum: an electrophysiological study of the catJ. Physiol 287 405CrossRefGoogle ScholarPubMed
Nicola, S. MSurmeier, JMalenka, R. C 2000 Dopaminergic modulation of neuronal excitability in the striatum and nucleus accumbensAnnu. Rev. Neurosci 23 185CrossRefGoogle ScholarPubMed
Nisenbaum, E. SBerger, T. WGrace, A. A 1993 Depression of glutamatergic and GABAergic synaptic responses in striatal spiny neurons by stimulation of presynaptic GABA-B receptorsSynapse 14 221CrossRefGoogle Scholar
Novak, K. E 2001 Neural control of discrete movement segments/the role of the cerebellum in the control and learning of movementsDoctoral thesis in Biomedical EngineeringEvanston, Northwestern UniversityGoogle Scholar
Novak, K. EMiller, L. EHouk, J. C 2000 Kinematic properties of rapid hand movements in knob turning taskExp. Brain Res 132 419CrossRefGoogle ScholarPubMed
Novak, K. EMiller, L. EHouk, J. C 2002 The use of overlapping submovements in the control of rapid hand movementsExp. Brain Res 144 351CrossRefGoogle ScholarPubMed
Novak, K. EMiller, L. EHouk, J. C 2003 Features of motor performance that drive adaptation in rapid hand movementsExp. Brain Res 148 388CrossRefGoogle ScholarPubMed
Ohta, HGunji, Y. P 2006 Recurrent neural network architecture with pre-synaptic inhibition for incremental learningNeural Networks 19 1106CrossRefGoogle ScholarPubMed
Pasupathy, AMiller, E. K 2005 Different time courses of learning-related activity in the prefrontal cortex and striatumNature 433 873CrossRefGoogle ScholarPubMed
Patterson, P. H 2007 Neuroscience. Maternal effects on schizophrenia riskScience 318 576CrossRefGoogle ScholarPubMed
Plenz, D 2003 When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal functionTINS 26 14427Google ScholarPubMed
Prescott, T. J 2005 Forced moves or good tricks in design space? Great moments in the evolution of the neural substrate for action selectionAdapt. Behav 15 9CrossRefGoogle Scholar
Preuss, T. M 1995 Do rats have prefrontal cortex? The Rose–Woolsey–Akert program reconsideredJ. Cogn. Neurosci 7 1CrossRefGoogle ScholarPubMed
Raymond, J. LLisberger, S. GMauk, M. D 1996 The cerebellum: a neuronal learning machine?Science 272 1126CrossRefGoogle ScholarPubMed
Redgrave, PPrescott, T. JGurney, K 1999 The basal ganglia: a vertebrate solution to the selection problem?Neuroscience 89 1009CrossRefGoogle ScholarPubMed
Roy, S. ABastianen, CNenonene, E 2003
Roy, STunik, EBastianen, C 2008 Firing patterns of GPi neurons associated with primary movements and corrective submovementsSociety for Neuroscience 2008 Washington D.CGoogle Scholar
Rubchinsky, L. LKopel, NSigvardt, K. A 2003 Modeling facilitation and inhibition of competing motor programs in basal ganglia subthalamic nucleus–pallidal circuitsPNAS 100 14427CrossRefGoogle ScholarPubMed
Sekerkova, GIlijic, EMugnaini, E 2004 Bromodeoxyuridine administered during neurogenesis of the projection neurons causes cerebellar defects in ratJ. Comp. Neurol 470 221CrossRefGoogle ScholarPubMed
Shadmehr, RMussa-Ivaldi, F. A 1994 Adaptive representation of dynamics during learning of a motor taskJ. Neurosci 14 3208CrossRefGoogle ScholarPubMed
Shi, LSmith, S. EMalkova, N 2009 Activation of the maternal immune system alters cerebellar development in the offspringBrain Behav. Immun 23 116CrossRefGoogle ScholarPubMed
Siddique, T 2007 Neurobiology of mental healthPak. J. Neurol. Sci 2 230Google Scholar
Smith, S. ELi, JGarbett, KMirnics, KPatterson, P. H 2007 Maternal immune activation alters fetal brain development through interleukin-6J. Neurosci 27 10695CrossRefGoogle ScholarPubMed
Smith, M. AShadmehr, R 2005 Intact ability to learn internal models of arm dynamics in Huntington's disease but not cerebellar degenerationJ. Neurophysiol 93 2809CrossRefGoogle Scholar
Stefan, MClaiborn, K. CStasiek, E 2005 Genetic mapping of putative Chrna7 and Luzp2 neuronal transcriptional enhancers due to impact of a transgene-insertion and .8 Mb deletion in a mouse model of Prader–Willi and Angelman syndromesBMC Genomics 6 157CrossRefGoogle Scholar
Sternad, DSchaal, S 1999 Segmentation of endpoint trajectories does not imply segmented controlExp. Brain Res. 124 118CrossRefGoogle Scholar
Sutton, R. SBarto, A. G 1998 Reinforcement Learning: An IntroductionCambridge, MAMIT PressGoogle Scholar
Tepper, J. MKoos, TWilson, C. J 2004 GABAergic microcircuits in the neostriatumTrends Neurosci 27 662CrossRefGoogle ScholarPubMed
Toni, IRowe, JStephan, K. EPassingham, R. E 2002 Changes of cortico-striatal effective connectivity during visuomotor learningCerebral Cortex 12 1040CrossRefGoogle ScholarPubMed
Tunik, EHouk, J. CGrafton, S. T 2009 Basal ganglia contribution to the initiation of corrective submovementsNeuroimage 47 1757CrossRefGoogle ScholarPubMed
Wang, JDam, GYildirim, S 2008 Reciprocity between the cerebellum and the cerebral cortex: nonlinear dynamics in microscopic modules for generating voluntary motor commandsComplexity 14 29CrossRefGoogle Scholar
Wang, LMamah, DHarms, M. P 2008 Progressive deformation of deep brain nuclei and hippocampal-amygdala formation in schizophreniaBiol. Psychiatry 64 1060CrossRefGoogle Scholar
Wise, S. P 2008 Forward frontal fields: phylogeny and fundamental functionTrends Neurosci 31 599CrossRefGoogle ScholarPubMed
Woodworth, R. S 1899 The accuracy of voluntary movementPsychol. Rev 3 1Google Scholar

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