Cortico-basal ganglia pathways are essential for the recall of well-established visuomotor associations

European Journal of Neuroscience

Volumn 20, Issue 11, 2004, Pages 3165-3178

  Nixon, Philip D ^a   McDonald, Kathryn R ^a,b   Gough, Patricia M ^a   Alexander, Iona H ^a   Passingham, Richard E ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Conditional motor learning; Excitotoxic lesions; Globus pallidus; Premotor cortex; Primates; Procedural learning

Indexed keywords

ANALYTICAL ERROR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASSOCIATION; BASAL GANGLION; BRAIN CORTEX; BRAIN INJURY; BRAIN REGION; CONTROLLED STUDY; GLOBUS PALLIDUS; HEMISPHERE; HYPOTHESIS; LEARNING; MACACA; MALE; NEUROIMAGING; NONHUMAN; PREFRONTAL CORTEX; PREMOTOR CORTEX; PRIMATE; PRIORITY JOURNAL; RECALL; RESPONSE TIME; TASK PERFORMANCE; VISUOMOTOR COORDINATION;

ANIMALS; ASSOCIATION LEARNING; BASAL GANGLIA; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; EXCITATORY AMINO ACID AGONISTS; FUNCTIONAL LATERALITY; KAINIC ACID; MACACA MULATTA; MALE; MENTAL RECALL; NEURAL NETWORKS (COMPUTER); NEURAL PATHWAYS; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; REACTION TIME;

EID: 10844259896     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03788.x     Document Type: Article

References (69)

1. Alamy, M., Trouche, E., Nieoullon, A. & Legallet, E. (1994) Globus pallidus and motor initiation: the bilateral effects of unilateral quisqualic acid-induced lesion on reaction times in monkeys. Exp. Brain Res., 99, 247-258.
2. Alexander, G.E., Crutcher, M.D. & DeLong, M.R. (1990) Basal ganglia-thalamocortical circuits: Parallel substrates for motor, oculomotor, 'prefrontal' and 'limbic' functions. In: Uylings, H.B.M., Van Eden, C.G., DeBruin, J.P.C., Corner, M.A. & Freenstra, M.P.G. (eds), Progress in Brain Research. Elsevier, pp. 119-146.
3. Boussaoud, D. & Kermadi, I. (1997) The primate striatum: neuronal activity in relation to spatial attention versus motor preparation. Eur. J. Neurosci., 9, 2152-2168.
4. Brasted, P.J., Bussey, T.J., Murray, E.A. & Wise, S.P. (2003) Role of the hippocampal system in associative learning beyond the spatial domain. Brain, 126, 1202-1223.
5. Brasted, P.J. & Wise, S.P. (2004) Comparison of learning-related neuronal activity in the dorsal premotor cortex and striatum. Eur. J. Neurosci, 19, 721-740.
6. Bussey, T.J., Wise, S.P. & Murray, E.A. (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.
7. Bussey, T.J., Wise, S.P. & Murray, E.A. (2002) Interaction of ventral and orbital prefrontal cortex with inferotemporal cortex in conditional visuomotor learning. Behav. Neurosci., 116, 703-715.
8. Canavan, A.G.M., Nixon, P.D. & Passingham, R.E. (1989) Motor learning in monkeys (Macaca fascicularis) with lesions in motor thalamus. Exp. Brain Res., 77, 113-126.
9. Deiber, M.-P., Passingham, R.E., Colebatch, J.G., Friston, K.J., Nixon, P.D. & Frackowiak, R.S.J. (1991) Cortical areas and the selection of movement: a study with positron emission tomography. Exp. Brain Res., 84, 393-402.
10. Deiber, M.-P., Wise, S.P., Honda, M., Catalan, M.J., Grafman, J. & Hallett, M. (1997) Frontal and parietal networks for conditional motor learning: a positron emission tomography study. J. Neurophysiol., 78, 977-991.
11. Denny-Brown, D. & Yanagisawa, N. (1976) The role of the basal ganglia in the initiation of movement. In: Yahr, M.D. (ed.), The Basal Ganglia. Raven Press, New York, pp. 116-149.
12. Eacott, M.J. & Gaffan, D. (1992) Inferotemporal-frontal disconnection: the uncinate fascicle and visual associative learning in monkeys. Eur. J. Neurosci., 4, 1320-1332.
13. Francois, C., Yelnik, J., Percheron, G. & Fenelon, G. (1994) Topographic distribution of the axonal endings from the sensorimotor and associative striatum in the macaque pallidum and substantia nigra. Exp. Brain Res., 102, 305-318.
14. Grafton, S.T., Fagg, A.M. & Arbib, M.A. (1998) Dorsal premotor cortex and conditional movement selection: a PET functional mapping study. J. Neurophysiol., 79, 1092-1097.
15. Grol, M., Verstraten, F., Passingham, R.E. & Toni, I. (2003) Posterior parietal contributions to the learning of visuomotor associations. Neuroimage, 19, S1076.
16. Hadj-Bouziane, F. & Boussaoud, D. (2003) Neuronal activity in the monkey striatum during conditional visuomotor learning. Exp. Brain Res., 153, 190-196.
17. Hadj-Bouziane, F., Meunier, M. & Boussaoud, D. (2003) Conditional visuomotor learning in primates: a key role for the basal ganglia. J. Physiol. Paris, 97, 567-579.
18. Halsband, U. & Passingham, R.E. (1985) Premotor cortex and the conditions for movement in monkeys (Macaca fascicularis). Behav. Brain Res., 18, 269-277.
19. Hikosaka, O., Nakamura, K., Sakai, K. & Nakahara, H. (2002) Central mechanisms of motor skill learning. Curr. Opin. Neurobiol., 12, 217-222.
20. Horak, F.B. & Anderson, M.E. (1984) Influence of globus pallidus on arm movements. I. Effects of kainic acid-induced lesions. J. Neurophysiol., 52, 290-304.
21. Ilinsky, I.A. & Kultas-Ilinsky, K. (1982) Stereotactic surgery in the rhesus monkey (Macaca mulatta) utilizing intracerebral landmarks. Appl. Neurophysiol., 45, 563-572.
22. Inase, M., Li, B.M., Takashima, I. & Iijima, T. (2001) Pallidal activity is involved in visuomotor association learning in monkeys. Eur. J. Neurosci., 14, 897-901.
23. Inase, M. & Tanji, J. (1994) Projections from the globus pallidus to the thalamic areas projecting to the dorsal area 6 of the macaque monkey: a multiple tracing study. Neurosci. Lett., 180, 135-137.
24. Kunzle, H. (1975) Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res., 88, 195-209.
25. Kunzle, H. (1978) An autoradiographic analysis of the efferent connections from premotor and adjacent prefrontal regions (areas 6 and 9) in macaca fascicularis. Brain Behav. Evol., 15, 185-234.
26. Kurata, K. (1994) Site of origin of projections from the thalamus to dorsal versus ventral aspects of the premotor cortex in monkeys. Neurosci. Res., 21, 71-76.
27. Kurata, K. & Hoffman, D.S. (1994) Differential effects of muscimol microinjection into dorsal and ventral aspects of the premotor cortex of monkeys. J. Neurophysiol., 71, 1151-1164.
28. Lawrence, A.D., Watkins, L.H.A., Sahakian, B.J., Hodges, J.R. & Robbins, T.W. (2000) Visual object and visuospatial cognition in Huntington's disease: implications for information processing in corticostriatal circuits. Brain, 123, 1349-1364.
29. Lu, M.-T., Preston, J.B. & Strick, P.L. (1994) Interconnections between the prefrontal cortex and the premotor areas in the frontal lobe. J. Comp. Neurol., 341, 375-392.
30. Luppino, G., Rozzi, S., Calzavara, R. & Matelli, M. (2003) Prefrontal and agranular cingulate projections to the dorsal premotor areas F2 and F7 in the macaque monkey. Eur. J. Neurosci., 17, 559-578.
31. Middleton, F.A. & Strick, P.L. (2000) Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res. Brain Res. Rev., 31, 236-250.
32. Middleton, F.A. & Strick, P.L. (2002) Basal-ganglia 'projections' to the prefrontal cortex of the primate. Cereb. Cortex, 12, 926-935.
33. Mink, J.W. & Thach, W.T. (1991) Basal ganglia motor control III. Pallidal ablation: normal reaction time, muscle cocontraction and slow movement. J. Neurophysiol., 65, 330-351.
34. Miyachi, S., Hikosaka, O., Miyashita, K., Karadi, Z. & Rand, M.K. (1997) Differential roles of monkey striatum in learning of sequential hand movement. Exp. Brain Res., 115, 1-5.
35. Miyachi, S., Hikosaka, O. & Xiaofeng, L. (2002) Differential activation of monkey striatal neurons in the early and late stages of procedural learning. Exp. Brain Res., 146, 122-126.
36. Murray, E.A., Bussey, T.J. & Wise, S.P. (2000) Role of prefrontal cortex in a network for arbitrary visuomotor mapping. Exp. Brain Res., 133, 114-129.
37. Nakahara, H., Doya, K. & Hikosaka, O. (2001) Parallel cortico-basal ganglia mechanisms for acquisition and execution of visuomotor sequences - a computational approach. J. Cogn. Neurosci., 13, 626-647.
38. Nixon, P.D. & Passingham, R.E. (2000) The cerebellum and cognition: cerebellar lesions impair sequence learning but not conditional visuomotor learning in monkeys. Neuropsychologia, 38, 1054-1072.
39. Nixon, P.D. & Passingham, R.E. (2001) Predicting sensory events: The role of the cerebellum in motor learning. Exp. Brain Res., 138, 251-257.
40. Parker, A. & Gaffan, D. (1998) Memory after frontal/temporal disconnection in monkeys: conditional and non-conditional tasks, unilateral and bilateral frontal lesions. Neuropsychologia, 36, 259-271.
41. Passingham, R.E. (1989) Premotor cortex and the retrieval of movement. Brain Behav. Evol., 33, 189-192.
42. Passingham, R.E. (1993) The Frontal Lobes and Voluntary Action. Oxford University Press, Oxford.
43. Pasupathy, A. & Miller, E.K. (2002) Comparison of neural activity in the prefrontal cortex and basal ganglia during conditional visuomotor learning. Program No. 285.10. Abstract Viewer/Itinerary Planner. Society for Neuroscience 2002, Washington DC, Online.
44. Paxinos, G., Huang, X.-U. & Toga, A.W. (2000) The Rhesus Monkey Brain in Stereotaxic Coordinates. Academic Press, San Diego.
45. Petrides, M. (1985) Deficits in non-spatial conditional associative learning after periarcuate lesions in the monkey. Behav. Brain Res., 16, 95-101.
46. Petrides, M. & Pandya, D.N. (2002) Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur. J. Neurosci., 16, 291-310.
47. Raichle, M.E., Fiez, J.A., Videen, T.O., MacLeod, A.K., Pardo, J.V., Fox, P.T. & Petersen, S.E. (1994) Practice related changes in human brain functional anatomy during non-motor learning. Cereb. Cortex, 4, 8-26.
48. Rushworth, M.F.S., Buckley, M.J., Gough, P., Hodinott-Hill, I., McDonald, K., Nixon, P.D. & Passingham, R.E. (2003) Attentional selection and action selection in the ventral prefrontal cortex. Program No. 722.11. Abstract Viewer/Itinerary Planner. Society for Neuroscience 2003, Washington DC, Online.
49. Saint-Cyr, J.A., Ungerleider, L.G. & Desimone, R. (1990) Organization of visual cortical inputs to the striatum and subsequent outputs to the pallidonigral complex in the monkey. J. Comp. Neurol., 298, 129-156.
50. Sambrook, M.A., Crossman, A.R., Mitchell, I., Robertson, R.G., Clarke, C.E. & Boyce, S. (1989) The basal ganglia mechanisms mediating primate models of movement disorders. In: Crossman, A.R. & Sambrook, M.A. (eds), Neural Mechanisms in Disorders of Movement. John Libbey, Eastleigh, Hants, UK, pp. 123-144.
51. Selemon, L.D. & Goldman-Rakic, P.S. (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J. Neurosci., 5, 776-794.
52. Selemon, L.D. & Goldman-Rakic, P.S. (1990) Topographic intermingling of striatonigral and striatopallidal neurons in the rhesus monkey. J. Comp. Neurol., 297, 359-376.
53. Tachibana, Y., Nambu, A., Hatanaka, N., Miyachi, S. & Takada, M. (2004) Input-output organization of the rostral part of the dorsal premotor cortex, with special reference to its corticostriatal projection. Neurosci. Res., 48, 45-57.
54. Takada, M., Nambu, A., Hatanaka, N., Tachibana, Y., Miyachi, S., Taira, M. & Inase, M. (2004) Organization of prefrontal outflow toward frontal motor-related areas in macaque monkeys. Eur J. Neurosci., 19, 3328-3342.
55. Toni, I. & Passingham, R.E. (1999) Prefrontal-basal ganglia pathways are involved in the learning of arbitrary visuomotor associations: a PET study. Exp. Brain Res., 127, 19-32.
56. Toni, I., Ramnani, N., Josephs, O., Ashburner, J. & Passingham, R.E. (2001) Learning arbitrary visuomotor associations: temporal dynamics of brain activity. Neuroimage, 14, 1048-1057.
57. Toni, I., Rowe, J., Stephan, K.E. & Passingham, R.E. (2002) Changes of Cortico-striatal Effective Connectivity during Visuomotor Learning. Cereb. Cortex, 12, 1040-1047.
58. Tremblay, L., Hollerman, J.R. & Schultz, W. (1998) Modifications of Reward Expectation-Related Neuronal Activity During Learning in Primate Striatum. J. Neurophysiol., 80, 964-977.
59. Trouche, E., Beaubaton, D., Amato, G., Viallet, F. & Legallet, E. (1984) Changes in reaction time after pallidal or nigral lesion in the monkey. In: Hassler, R.G. & Christ, J.F. (eds), Advances in Neurology. Raven Press, New York, pp. 29-38.
60. Tucker, J., Harding, A.E., Jahanshahi, M., Nixon, P.D., Rushworth, M., Quinn, N.P. & Thompson, P.D. (1996) Associative learning in patients with cerebellar ataxia. Behav. Neurosci., 110, 1-6.
61. Wallis, J.D. & Miller, E.K. (2003) From rule to response: neuronal processes in the premotor and prefrontal cortex. J. Neurophysiol., 90, 1790-1806.
62. Wang, Y., Shima, K., Isoda, M., Sawamura, H. & Tanji, J. (2002) Spatial distribution and density of prefrontal cortical cells projecting to three sectors of the premotor cortex. Neuroreport, 13, 1341-1344.
63. Wang, M., Zhang, H. & Li, B.-M. (2000) Deficit in conditional visuomotor learning by local infusion of bicuculline into the ventral prefrontal cortex in monkeys. Eur. J. Neurosci., 12, 3787-3796.
64. Webster, M.J., Bachevalier, J. & Ungerleider, L.G. (1993) Subcortical connections of inferior temporal areas TE and TEO in macaque monkeys. J. Comp. Neurol., 335, 73-91.
65. Webster, M.J., Bachevalier, J. & Ungerleider, L.G. (1994) Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb. Cortex, 4, 470-483.
66. Wise, S.P. (1996a) Evolution of neuronal activity during conditional motor learning. In: Bloedel, R., Ebner, T. & Wise, S. (eds), The Acquisition of Motor Behavior in Vertebrates. MIT Press, pp. 261-286.
67. Wise, S.P. (1996b) The role of the basal ganglia in procedural memory. Semin. Neurosci., 8, 39-46.
68. Wise, S.P. & Murray, E.A. (1999) Role of the hippocampal system in conditional motor learning: Mapping antecedents to action. Hippocampus, 9, 101-117.
69. Wise, S.P. & Murray, E.A. (2000) Arbitrary associations between antecedents and actions. Trends Neurosci., 23, 271-276.