Modulation of neuronal activity in the monkey putamen associated with changes in the habitual order of sequential movements

Journal of Neurophysiology

Volumn 104, Issue 3, 2010, Pages 1355-1369

  Deffains, Marc ^a   Legallet, Eric ^a   Apicella, Paul ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CHOLINERGIC SYSTEM; CONTROLLED STUDY; CORPUS STRIATUM; CORRELATION ANALYSIS; INTERNEURON; LEARNING; MALE; MONKEY; MOVEMENT (PHYSIOLOGY); NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PUTAMEN; SACCADIC EYE MOVEMENT; STIMULUS RESPONSE; TASK PERFORMANCE;

ANIMALS; HABITUATION, PSYCHOPHYSIOLOGIC; HAPLORHINI; LEARNING; MACACA FASCICULARIS; MALE; MOVEMENT; NEURONS; PHOTIC STIMULATION; PSYCHOMOTOR PERFORMANCE; PUTAMEN; RANDOM ALLOCATION;

EID: 77957194858     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00355.2010     Document Type: Article

References (59)

1. + conductance in rat neostriatal neurons. Nature 344: 240-242, 1990.
2. Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia. Trends Neurosci 12: 366-374, 1989.
3. Alexander GE, Crutcher MD. Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J Neurophysiol 64: 133-150, 1990. (Pubitemid 20206363)
4. Apicella P. Tonically active neurons in the primate striatum and their role in the processing of information about motivationally relevant events. Eur J Neurosci 16: 2017-2026, 2002. (Pubitemid 35454246)
5. Apicella P. Leading tonically active neurons of the striatum from reward detection to context recognition. Trends Neurosci 30: 299-306, 2007. (Pubitemid 46802832)
6. Apicella P, Deffains M, Ravel S, Legallet E. Tonically active neurons in the striatum differentiate between delivery and omission of expected reward in a probabilistic task context. Eur J Neurosci 30: 515-526, 2009.
7. Apicella P, Scarnati E, Ljungberg T, Schultz W. Neuronal activity in monkey striatum related to the expectation of predictable environmental events. J Neurophysiol 68: 945-960, 1992.
8. Balleine BW, Liljeholm M, Ostlund SB. The integrative function of the basal ganglia in instrumental conditioning. Behav Brain Res 199: 43-52, 2009.
9. Bar-Gad I, Morris G, Bergman H. Information processing, dimensionality reduction and reinforcement learning in the basal ganglia. Prog Neurobiol 71: 439-473, 2003.
10. Barnes TD, Kubota Y, Hu D, Jin DZ, Graybiel AM. Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories. Nature 437: 1158-1161, 2005.
11. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G. Acetylcholine-mediated modulation of striatal functions. Trends Neurosci 23: 120-126, 2000.
12. Carelli RM, Wolske M, West MO. Loss of lever press-related firing of rat striatal forelimb neurons after repeated sessions in a lever pressing task. J Neurosci 17: 1804-1814, 1997.
13. Crutcher MD, Alexander GM. Movement-related neuronal activity selectively coding either direction or muscle pattern in three motor areas of the monkey. J Neurophysiol 64: 151-163, 1990.
14. Crutcher MD, DeLong MR. Single cell studies of the primate putamen. II. Relations to direction of movement and pattern of muscular activity. Exp Brain Res 53: 244-258, 1984.
15. Dominey PF. A shared system for learning serial and temporal structure of sensorimotor sequences? Evidence from simulation and human experiments. Cogn Brain Res 6: 163-172, 1998.
16. Doyon J, Bellec P, Amsel R, Penhune V, Monchi O, Carrier J, Lehéricy S, Benali H. Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res 199: 61-75, 2009.
17. Doyon J, Penhune V, Ungerleider LG. Distinct contribution of the corticostriatal and cortico-cerebellar systems to motor skill learning. Neuropsychologia 41: 252-262, 2003. (Pubitemid 35365955)
18. Fitts PM. Perceptual-motor skill learning. In: Categories of Human Learning, edited by Melton AW. New York: Academic, 1964, p. 243-285.
19. Floyer-Lea A, Matthews PM. Changing brain networks for visuomotor control with increased movement automaticity. J Neurophysiol 92: 2405-2412, 2004. (Pubitemid 39298692)
20. Graybiel AM. Building action repertoires: memory and learning functions of the basal ganglia. Curr Op Neurobiol 5: 733-741, 1998.
21. Hay JF, Moscovitch M, Levine B. Dissociating habit and recollection: evidence from Parkinson's disease, amnesia and focal lesion patients. Neuropsychologia 40: 1324-1334, 2002. (Pubitemid 34249842)
22. Hikosaka O, Nakahara H, Rand MK, Sakai K, Lu X, Nakamura K, Miyachi S, Doya K. Parallel neural networks for learning sequential procedures. Trends Neurosci 22: 464-470, 1999.
23. Hikosaka O, Sakamoto M, Usui S. Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J Neurophysiol 61: 814-832, 1989. (Pubitemid 19111973)
24. Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM. Building neural representations of habits. Science 286: 1745-1749, 1999.
25. Joshua M, Adler A, Mitelman R, Vaadia E, Bergman H. Midbrain dopaminergic neurons and striatal cholinergic interneurons encode the difference between reward and aversive events at different epochs of probabilistic classical conditioning trials. J Neurosci 28: 11673-11684, 2008.
26. Jueptner M, Frith CD, Brooks DJ, Frackowiak RSJ, Passingham RE. Anatomy of motor learning. II. Subcortical structures and learning by trial and error. J Neurophysiol 77: 1325-1337, 1997.
27. Kimura M. Behaviorally contingent property of movement-related activity of the primate putamen. J Neurophysiol 63: 1277-1296, 1990.
28. Kimura M, Rajkowski J, Evarts EV. Tonically discharging putamen neurons exhibit set dependent responses. Proc Natl Acad Sci USA 81: 4998-5001, 1984. (Pubitemid 14066241)
29. Knowlton BJ, Mangels JA, Squire LR. A neostriatal habit learning system in humans. Science 273: 1399-1402, 1996.
30. Kubota Y, Liu J, DeCoteau WE, Eden UT, Smith AC, Graybiel AM. Stable encoding of task structure coexists with flexible coding of task events in sensorimotor striatum. J Neurophysiol 102: 2142-2160, 2009.
31. Lee D, Quessy S. Activity in the supplementary motor area related to learning and performance during a sequential visuomotor task. J Neurophysiol 89: 1039-1056, 2003. (Pubitemid 36206150)
32. Lee IH, Seitz AR, Assad JA. Activity of tonically active neurons in the monkey putamen during initiation and withholding of movement. J Neurophysiol 95: 2391-2403, 2006.
33. Lehéricy S, Benali H, Van de Moortele PF, Pélégrini- Issac M, Waechter T, Ugurbil K, Doyon J. Distinct basal ganglia territories are engaged in early and advanced motor sequence learning. Proc Natl Acad Sci USA 102: 12566-12571, 2005. (Pubitemid 41266399)
34. Logan GD. Toward an instance theory of automatization. Psychol Rev 95: 492-527, 1988.
35. Matsumoto N, Hanakawa T, Maki S, Graybiel AM, Kimura M. Role of nigrostriatal dopamine system in learning to perfrom sequential motor tasks in a predictive manner. J Neurophysiol 82: 978-998, 1999. (Pubitemid 29387869)
36. Matsuzaka Y, Picard N, Strick PL. Skill representation in the primary motor cortex after long-term practice. J Neurophysiol 97: 1819-1832, 2007.
37. Mink JW. The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol 50: 381-425, 1996.
38. Mishkin M, Malamut B, Bachevalier J. Memories and habits: two neural systems. In: Neurobiology of Learning and Memory, edited by Lynch G, McGaugh JL, Weinberger NM. New York: Guilford, 1984, p. 65-77.
39. Miyachi S, Hikosaka O, Lu X. Differential activation of monkey striatal neurons in the early and late stages of procedural learning. Exp Brain Res 146: 122-126, 2002.
40. Miyashita K, Rand MK, Miyachi S, Hikosaka O. Anticipatory saccades in sequential procedural learning in monkeys. J Neurophysiol 76: 1361-1366, 1996.
41. Nambu A, Kaneda K, Tokuno H, Takada M. Organization of corticostriatal motor inputs in monkey putamen. J Neurophysiol 88: 1830-1842, 2002.
42. Nissen MJ, Bullemer P. Attentional requirements of learning: evidence from performance measures. Cogn Psychol 19: 1-32, 1987.
43. Nixon PD, Passingham RE. The cerebellum and cognition: cerebellar lesions impair sequence learning but not conditional visuomotor learning in monkeys. Neuropsychologia 38: 1054-1072, 2000.
44. Packard MG, Knowlton BJ. Learning and memory functions of the basal ganglia. Annu Rev Neurosci 25: 563-593, 2002. (Pubitemid 34748029)
45. Poldrack RA, Sabb FW, Foerde K, Tom SM, Asarnow RF, Bookheimer SY, Knowlton BJ. The neural correlates of motor skill automaticity. J Neurosci 25: 5356-5364, 2005. (Pubitemid 40770915)
46. Procyk E, Dominey PF, Amiez C, Joseph JP. The effects of sequence structure and reward schedule on serial reaction time learning in the monkey. Cogn Brain Res 9: 239-248, 2000. (Pubitemid 30243109)
47. Ravel S, Sardo P, Legallet E, Apicella P. Influence of spatial information on responses of tonically active neurons in the monkey striatum. J Neurophysiol 95: 2975-2986, 2006.
48. Romo R, Scarnati E, Schultz W. Role of primate basal ganglia and frontal cortex in the internal generation of movements. II. Movement-related activity in the anterior striatum. Exp Brain Res 91: 385-395, 1992.
49. Sardo P, Ravel S, Legallet E, Apicella P. Influence of the predicted time of stimuli eliciting movements on responses of tonically active neurons in the monkey striatum. Eur J Neurosci 12: 1801-1816, 2000.
50. Shimo Y, Hikosaka O. Role of tonically active neurons in primate caudate in reward-oriented saccadic eye movement. J Neurosci 21: 7804-7814, 2001.
51. Schultz W, Romo R. Role of primate basal ganglia and frontal cortex in the internal generation of movements. I. Preparatory activity in the anterior striatum. Exp Brain Res 91: 363-384, 1992.
52. Schultz W, Tremblay L, Hollerman JR. Changes in behavior-related neuronal activity in the striatum during learning. Trends Neurosci 26: 321-328, 2003. (Pubitemid 36694320)
53. Stadler MA. The role of attention in implicit learning. J Exp Psychol Learn Mem Cogn 21: 674-685, 1995.
54. Szabo J, Cowan WM. A stereotaxic atlas of the brain of the cynomolgus monkey (Macaca fascicularis). J Comp Neurol 222: 265-300, 1984.
55. Takada M, Tokuno H, Nambu A, Inase M. Corticostriatal projections from the somatic motor areas of the frontal cortex in the macaque monkey: segregation versus overlap of input zones from the primary motor cortex, the supplementary motor area, and the premotor cortex. Exp Brain Res 120: 114-128, 1998. (Pubitemid 28212026)
56. Tang C, Pawlak AP, Prokopenko V, West MO. Changes in activity of the striatum during formation of a motor habit. Eur J Neurosci 25: 1212-1227, 2007.
57. Wu T, Hallett M. A functional MRI study of automatic movements in patients with Parkinson's disease. Brain 128: 2250-2259, 2005. (Pubitemid 41407965)
58. Yamada H, Matsumoto N, Kimura M. Tonically active neurons in the primate caudate nucleus and putamen differentially encode instructed motivational outcomes of action. J Neurosci 24: 3500-3510, 2004. (Pubitemid 38481106)
59. Yin HH, Knowlton BJ. The role of the basel ganglia in habit formation. Nat Rev Neurosci 7: 464-476, 2006.