Skip to main content
Log in

Comparison of population activity in the dorsal premotor cortex and putamen during the learning of arbitrary visuomotor mappings

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

A previous study found that as monkeys learned novel mappings between visual cues and responses, neuronal activity patterns evolved at approximately the same time in both the dorsal premotor cortex (PMd) and the putamen. Here we report that, in both regions, the population activity for novel mappings came to resemble that for familiar ones as learning progressed. Both regions showed activity differences on trials with correct responses versus those with incorrect ones. In addition to these common features, we observed two noteworthy differences between PMd and putamen activity during learning. After a response choice had been made, but prior to feedback about the correctness of that choice (reward or nonreward), the putamen showed a sustained activity increase in activity, whereas PMd did not. Also in the putamen, this prereward activity was highly selective for the specific visuomotor mapping that had just been performed, and this selectivity was maintained until the time of the reward. After performance reached an asymptote, the degree of this selectivity decreased markedly to the level typical for familiar visuomotor mappings. These findings support the hypothesis that neurons in the striatum play a pivotal role in associative learning.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Asaad WF, Rainer G, Miller EK (1998) Neural activity in the primate prefrontal cortex during associative learning. Neuron 21:1399–1407

    Article  PubMed  CAS  Google Scholar 

  • Barefoot HC, Baker HF, Ridley RM (2002) Crossed unilateral lesions of temporal lobe structures and cholinergic cell bodies impair visual conditional and object discrimination learning in monkeys. Eur J Neurosci 15:507–516

    Article  PubMed  CAS  Google Scholar 

  • Barefoot HC, Maclean CJ, Baker HF, Ridley RM (2003) Unilateral hippocampal and inferotemporal cortex lesions in opposite hemispheres impair learning of single-pair visual discriminations as well as visuovisual conditional tasks in monkeys. Behav Brain Res 141:51–62

    Article  PubMed  Google Scholar 

  • Bar-Gad I, Bergman H (2001) Stepping out of the box: information processing in the neural networks of the basal ganglia. Curr Opin Neurobiol 11:689–695

    Article  PubMed  CAS  Google Scholar 

  • Bar-Gad I, Havazelet-Heimer G, Goldberg JA, Ruppin E, Bergman H (2000) Reinforcement-driven dimensionality reduction—a model for information processing in the basal ganglia. J Basic Clin Physiol Pharmacol 11:305–320

    PubMed  CAS  Google Scholar 

  • Berger B, Trottier S, Verney C, Gaspar P, Alvarez C (1988) Regional and laminar distribution of the dopamine and serotonin innervation in the macaque cerebral cortex: a radioautographic study. J Comp Neurol 273:99–119

    Article  PubMed  CAS  Google Scholar 

  • Brasted PJ, Wise SP (2004) Comparison of learning-related neuronal activity in the dorsal premotor cortex and striatum. Eur J Neurosci 19:721–740

    Article  PubMed  Google Scholar 

  • Brasted PJ, Bussey TJ, Murray EA, Wise SP (2002) Fornix transection impairs conditional visuomotor learning in tasks involving nonspatially differentiated responses. J Neurophysiol 87:631–633

    PubMed  Google Scholar 

  • Brasted PJ, Bussey TJ, Murray EA, Wise SP (2003) Role of the hippocampal system in associative learning beyond the spatial domain. Brain 126:1202–1223

    Article  PubMed  CAS  Google Scholar 

  • Bussey TJ, Wise SP, Murray EA (2001) The role of ventral and orbital prefrontal cortex in conditional visuomotor learning and strategy use in rhesus monkeys (Macaca mulatta). Behav Neurosci 115:971–982

    Article  PubMed  CAS  Google Scholar 

  • Bussey TJ, Wise SP, Murray EA (2002) Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning. Behav Neurosci 116:703–715

    Article  PubMed  Google Scholar 

  • Cahusac PM, Rolls ET, Miyashita Y, Niki H (1993) Modification of the responses of hippocampal neurons in the monkey during the learning of a conditional spatial response task. Hippocampus 3:29–42

    Article  PubMed  CAS  Google Scholar 

  • Canavan AGM, Nixon PD, Passingham RE (1989) Motor learning in monkeys (Macaca fascicularis) with lesions in motor thalamus. Exp Brain Res 77:113–126

    Article  PubMed  CAS  Google Scholar 

  • Chen LL, Wise SP (1995a) Neuronal activity in the supplementary eye field during acquisition of conditional oculomotor associations. J Neurophysiol 73:1101–1121

    PubMed  CAS  Google Scholar 

  • Chen LL, Wise SP (1995b) Supplementary eye field contrasted with the frontal eye field during acquisition of conditional oculomotor associations. J Neurophysiol 73:1122–1134

    PubMed  CAS  Google Scholar 

  • Crutcher MD, DeLong MR (1984) Single cell studies of the primate putamen. II Relations to direction of movement and pattern of muscular activity. Exp Brain Res 53:244–258

    Article  PubMed  CAS  Google Scholar 

  • Deiber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RS (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 84:393–402

    Article  PubMed  CAS  Google Scholar 

  • Deiber MP, Wise SP, Honda M, Catalan MJ, Grafman J, Hallett M (1997) Frontal and parietal networks for conditional motor learning: a positron emission tomography study. J Neurophysiol 78:977–991

    PubMed  CAS  Google Scholar 

  • Djurfeldt M, Ekeberg O, Graybiel A (2001) Cortex–basal ganglia interaction and attractor states. Neurocomputing 38–40:573–579

    Article  Google Scholar 

  • Eacott MJ, Gaffan D (1992) Inferotemporal-frontal disconnection: the uncinate fascicle and visual associative learning in monkeys. Eur J Neurosci 4:1320–1332

    Article  PubMed  Google Scholar 

  • Eliassen JC, Souza T, Sanes JN (2003) Experience-dependent activation patterns in human brain during visual-motor associative learning. J Neurosci 23:10540–10547

    PubMed  CAS  Google Scholar 

  • Fiorillo CD, Tobler PN, Schultz W (2003) Discrete coding of reward probability and uncertainty by dopamine neurons. Science 299:1898–1902

    Article  PubMed  CAS  Google Scholar 

  • Gaffan D, Harrison S (1988) Inferotemporal-frontal disconnection and fornix transection in visuomotor conditional learning by monkeys. Behav Brain Res 31:149–163

    Article  PubMed  CAS  Google Scholar 

  • Gaspar P, Stepniewska I, Kaas JH (1992) Topography and collateralization of the dopaminergic projections to motor and lateral prefrontal cortex in owl monkeys. J Comp Neurol 325:1–21

    Article  PubMed  CAS  Google Scholar 

  • Groves PM (1983) A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement. Brain Res Rev 5:109–132

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hadj-Bouziane F, Boussaoud D (2003) Neuronal activity in the monkey striatum during conditional visuomotor learning. Exp Brain Res 153:190–196

    Article  PubMed  Google Scholar 

  • Hadj-Bouziane F, Meunier M, Boussaoud D (2003) Conditional visuo-motor learning in primates: a key role for the basal ganglia. J Physiol (Paris) 97:567–579

    Article  Google Scholar 

  • Halsband U, Passingham RE (1985) Premotor cortex and the conditions for a movement in monkeys. Behav Brain Res 18:269–277

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Hollerman JR, Tremblay L, Schultz W (1998) Influence of reward expectation on behavior-related neuronal activity in primate striatum. J Neurophysiol 80:947–963

    PubMed  CAS  Google Scholar 

  • Houk JC, Wise SP (1995) Distributed modular architectures linking basal ganglia, cerebellum, and cerebral cortex: their role in planning and controlling action. Cereb Cortex 5:95–110

    Article  PubMed  CAS  Google Scholar 

  • Houk JC, Keifer J, Barto AG (1993) Distributed motor commands in the limb premotor network. Trends Neurosci 16:27–33

    Article  PubMed  CAS  Google Scholar 

  • Houk JC, Adams JL, Barto AG (1995) A model of how the basal ganglia generate and use neural signals that predict reinforcement. In: Houk JC, Davis JL, Beiser DG (eds) Models of information processing in the basal ganglia. MIT, Cambridge, pp 249–270

    Google Scholar 

  • Inase M, Li BM, Takashima I, Iijima T (2001) Pallidal activity is involved in visuomotor association learning in monkeys. Eur J Neurosci 14:897–901

    Article  PubMed  CAS  Google Scholar 

  • Ito S, Stuphorn V, Brown JW, Schall JD (2003) Performance monitoring by the anterior cingulate cortex during saccade countermanding. Science 302:120–122

    Article  PubMed  CAS  Google Scholar 

  • Itoh H, Nakahara H, Hikosaka O, Kawagoe R, Takikawa Y, Aihara K (2003) Correlation of primate caudate neural activity and saccade parameters in reward-oriented behavior. J Neurophysiol 89:1774–1783

    Article  PubMed  Google Scholar 

  • Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM (1999) Building neural representations of habits. Science 286:1745–1749

    Article  PubMed  CAS  Google Scholar 

  • Kawagoe R, Takikawa Y, Hikosaka O (2004) Reward-predicting activity of dopamine and caudate neurons. A possible mechanism of motivational control of saccadic eye movement. J Neurophysiol 91:1013–1024

    Article  PubMed  CAS  Google Scholar 

  • Kawato M (1989) Adaptation and learning in control of voluntary movement by the central nervous system. Adv Robotics 3:229–249

    Google Scholar 

  • Laubach M, Wessberg J, Nicolelis MA (2000) Cortical ensemble activity increasingly predicts behaviour outcomes during learning of a motor task. Nature 405:567–571

    Article  PubMed  CAS  Google Scholar 

  • Lewis DA, Campbell MJ, Foote SL, Goldstein M, and Morrison JH (1987) The distribution of tyrosine hydroxylase-immunoreactive fibers in primate neocortex is widespread but regionally specific. J Neurosci 7:279–290

    PubMed  CAS  Google Scholar 

  • Mauritz KH, Wise SP (1986) Premotor cortex of the rhesus monkey: neuronal activity in anticipation of predictable environmental events. Exp Brain Res 61:229–244

    Article  PubMed  CAS  Google Scholar 

  • Mink JW (1996) The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50:381–425

    Article  PubMed  CAS  Google Scholar 

  • Mitz AR, Godschalk M, Wise SP (1991) Learning-dependent neuronal activity in the premotor cortex: activity during the acquisition of conditional motor associations. J Neurosci 11:1855–1872

    PubMed  CAS  Google Scholar 

  • Moody SL, Wise SP, di Pellegrino G, Zipser D (1998) A model that accounts for activity in primate frontal cortex during a delayed matching-to-sample task. J Neurosci 18:399–410

    PubMed  CAS  Google Scholar 

  • Murray EA, Wise SP (1996) Role of the hippocampus plus subjacent cortex but not amygdala in visuomotor conditional learning in rhesus monkeys. Behav Neurosci 110:1261–1270

    Article  PubMed  CAS  Google Scholar 

  • Murray EA, Brasted PJ, Wise SP (2002) Arbitrary sensorimotor mapping and the life of primates. In: Squire LR, Schacter DL (eds) Neuropsychology of memory. Guilford, New York, pp 339–348

    Google Scholar 

  • Nicolelis MAL, Dimitrov D, Carmena JM, Crist R, Lehew G, Kralik JD, Wise SP (2003) Chronic, multisite, multielectrode recordings in macaque monkeys. Proc Nat Acad Sci USA 100:11041–11046

    Article  PubMed  CAS  Google Scholar 

  • Nixon PD, McDonald KR, Gough PM, Alexander IH, Passingham RE (2004) Cortico-basal ganglia pathways are essential for the recall of well-established visuomotor associations. Eur J Neurosci 20:3165–3178

    Article  PubMed  Google Scholar 

  • Pasupathy A, Miller EK (2005) Different time courses for learning-related activity in the prefrontal cortex and striatum. Nature 433:873–876

    Article  PubMed  CAS  Google Scholar 

  • Paus T, Petrides M, Evans AC, Meyer E (1993) Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. J Neurophysiol 70:453–469

    PubMed  CAS  Google Scholar 

  • Petrides M (1985) Deficits in non-spatial conditional associative learning after periarcuate lesions in the monkey. Behav Brain Res 16:95–101

    Article  PubMed  CAS  Google Scholar 

  • Ridley RM, Baker HF (1997) Evidence for a specific information processing deficit in monkeys with lesions of the septo-hippocampal system. Cortex 33:167–176

    PubMed  CAS  Google Scholar 

  • Roesch MR, Olson CR (2004) Neuronal activity related to reward value and motivation in primate frontal cortex. Science 304:307–310

    Article  PubMed  CAS  Google Scholar 

  • Rupniak NMJ, Gaffan D (1987) Monkey hippocampus and learning about spatially directed movements. J Neurosci 7:2331–2337

    PubMed  CAS  Google Scholar 

  • Schall JD, Stuphorn V, Brown JW (2002) Monitoring and control of action by the frontal lobes. Neuron 36:309–322

    Article  PubMed  CAS  Google Scholar 

  • Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1–27

    PubMed  CAS  Google Scholar 

  • Schultz W (2004) Neural coding of basic reward terms of animal learning theory, game theory, microeconomics and behavioural ecology. Curr Opin Neurobiol 14:139–147

    Article  PubMed  CAS  Google Scholar 

  • Schultz W, Tremblay L, Hollerman JR (2003) Changes in behavior-related neuronal activity in the striatum during learning. Trends Neurosci 26:321–328

    Article  PubMed  CAS  Google Scholar 

  • Shohamy D, Myers CE, Grossman S, Sage J, Gluck MA, Poldrack RA (2004) Cortico-striatal contributions to feedback-based learning: converging data from neuroimaging and neuropsychology. Brain 127:851–859

    Article  PubMed  CAS  Google Scholar 

  • Siegel S, Castellan NJ (1988) Nonparametric statistics for the behavioral sciences. McGraw-Hill, New York

    Google Scholar 

  • Suri RE, Schultz W (1999) A neural network model with dopamine-like reinforcement signal that learns a spatial delayed response task. Neuroscience 91:871–890

    Article  PubMed  CAS  Google Scholar 

  • Suri RE, Bargas J, Arbib MA (2001) Modeling functions of striatal dopamine modulation in learning and planning. Neuroscience 103:65–85

    Article  PubMed  CAS  Google Scholar 

  • Takikawa Y, Kawagoe R, Hikosaka O (2004) A possible role of midbrain dopamine neurons in short- and long-term adaptation of saccades to position-reward mapping. J Neurophysiol 92:2520–2529

    Article  PubMed  Google Scholar 

  • Thoroughman KA, Shadmehr R (1999) Electromyographic correlates of learning an internal model of reaching movements. J Neurosci 19:8573–8588

    PubMed  CAS  Google Scholar 

  • Toni I, Passingham RE (1999) Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study. Exp Brain Res 127:19–32

    Article  PubMed  CAS  Google Scholar 

  • Toni I, Ramnani N, Josephs O, Ashburner J, Passingham RE (2001) Learning arbitrary visuomotor associations: temporal dynamic of brain activity. Neuroimage 14:1048–1057

    Article  PubMed  CAS  Google Scholar 

  • Toni I, Rowe J, Stephan KE, Passingham RE (2002) Changes of cortico-striatal effective connectivity during visuomotor learning. Cereb Cortex 12:1040–1047

    Article  PubMed  Google Scholar 

  • Tremblay L, Hollerman JR, Schultz W (1998) Modifications of reward expectation-related neuronal activity during learning in primate striatum. J Neurophysiol 80:964–977

    PubMed  CAS  Google Scholar 

  • Turner RS, DeLong MR (2000) Corticostriatal activity in primary motor cortex of the macaque. J Neurosci 20:7096–7108

    PubMed  CAS  Google Scholar 

  • Waelti P, Dickinson A, Schultz W (2001) Dopamine responses comply with basic assumptions of formal learning theory. Nature 412:43–48

    Article  PubMed  CAS  Google Scholar 

  • Wang M, Zhang H, Li BM (2000) Deficit in conditional visuomotor learning by local infusion of bicuculline into the ventral prefrontal cortex in monkeys. Eur J Neurosci 12:3787–3796

    Article  PubMed  CAS  Google Scholar 

  • Williams SM, Goldman-Rakic PS (1993) Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. Cerebral Cortex 3:199–222

    Article  PubMed  CAS  Google Scholar 

  • Wirth S, Yanike M, Frank LM, Smith AC, Brown EN, Suzuki WA (2003) Single neurons in the monkey hippocampus and learning of new associations. Science 300:1578–1581

    Article  PubMed  CAS  Google Scholar 

  • Wise SP, Murray EA (1999) Role of the hippocampal system in conditional motor learning: mapping antecedents to action. Hippocampus 9:101–117

    Article  PubMed  CAS  Google Scholar 

  • Zheng T, Wilson CJ (2002) Corticostriatal combinatorics: the implications of corticostriatal axonal arborizations. J Neurophysiol 87:1007–1017

    PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We thank Mr. Jim Fellows for assistance with behavioral training and Dr. Andrew R. Mitz for technical and engineering support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Steven P. Wise.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buch, E.R., Brasted, P.J. & Wise, S.P. Comparison of population activity in the dorsal premotor cortex and putamen during the learning of arbitrary visuomotor mappings. Exp Brain Res 169, 69–84 (2006). https://doi.org/10.1007/s00221-005-0130-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-005-0130-y

Keywords

Navigation