Implementation of action sequences by a neostriatal site: A lesion mapping study of grooming syntax

Journal of Neuroscience

Volumn 16, Issue 10, 1996, Pages 3444-3458

  Cromwell, Howard C ^a,b   Berridge, Kent C ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

basal ganglia; excitotoxin; globus pallidus; grooming; lesion; movement; neostriatum; neuroethology; pallidum; quinolinic acid; sensorimotor; sequence; serial order; stereology; syntax

Indexed keywords

EXCITOTOXIN; QUINOLINIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN MAPPING; CELL DEATH; GLOBUS PALLIDUS; GROOMING; MALE; MOVEMENT (PHYSIOLOGY); NEOSTRIATUM; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORIMOTOR FUNCTION; STEREOLOGY;

EID: 0029881870     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.16-10-03444.1996     Document Type: Article

References (125)

1. Agostino R, Beradelli A, Formica A, Accornero N, Manfredi M (1992) Sequential arm movements in patients with Parkinson's disease, Huntington's disease and dystonia. Brain 115:1481-1495.
2. Albin RL, Reiner A, Anderson KD, Penney JB, Young AB (1990) Striatal and nigral neuron subpopulations in rigid Huntington's disease: implications for the functional anatomy of chorea and rigidity-akinesia. Ann Neurol 27:357-365.
3. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375.
4. Aldridge JW, Berridge KC, Herman M, Zimmer L (1993) Neuronal coding of serial order: syntax of grooming in the neostriatum. Psychol Sci 4:391-395.
5. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357-381.
6. Alheid GF, Heimer L (1988) New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: the striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience 27:1-39.
7. Bakshi VP, Kelley AE (1993) Striatal regulation of morphine-induced hyperphagia: an anatomical mapping study. Psychopharmacology 111:207-214.
8. Baunez C, Nieoullon A, Amalric M (1995) Dopamine and complex sensorimotor integration: further studies in a conditioned motor task in the rat. Neuroscience 65:375-384.
9. Beckstead RM (1983) A reciprocal axonal connection between the subthalamic nucleus and the neostriatum in the cat. Brain Res 275:137-142.
10. Benecke R, Rothwell JC, Dick JP, Day BL, Marsden CD (1987) Disturbance of sequential movements in patients with Parkinson's disease. Brain 110:361-379.
11. Berntson GG, JF Jang, Ronica AE (1988) Brainstem system and grooming behaviors. Ann NY Acad Sci 525:350-362.
12. Berridge KC (1989a) Progressive degradation of serial grooming chains by descending decerebration. Behav Brain Res 33:241-253.
13. Berridge KC (1989b) Substantia nigra 6-OHDA lesions mimic striatopallidal disruption of syntactic grooming chains: a neural systems analysis of sequence control. Psychobiology 17:377-385.
14. Berridge KC (1990) Comparative fine structure of action: rules of form and sequence in the grooming patterns of six rodent species. Behavior 113:1-22.
15. Berridge KC, Cromwell HC (1990) Motivational-sensorimotor interaction controls aphagia and exaggerated treading after striatopallidal lesions. Behav Neurosci 104:778-795.
16. Berridge KC, Fentress JC (1986) Contextual control of trigeminal sensorimotor function. J Neurosci 9:325-330.
17. Berridge KC, Fentress JC (1987) Disruption of natural grooming chains after striatopallidal lesions. Psychobiology 15:336-342.
18. Berridge KC, Whishaw IQ (1992) Cortex, striatum and cerebellum: control of serial order in a grooming sequence. Exp Brain Res 90:275-290.
19. Berridge KC, Fentress JC, Parr H (1987) Natural syntax rules control action sequence of rats. Behav Brain Res 23:59-68.
20. Bhatia KP, Marsden CD (1994) The behavioral and motor consequences of focal lesions of the basal ganglia in man. Brain 117:859-876.
21. Bradshaw JL, Phillips JG, Dennis C, Mattingley JB, Andrewes D, Chiu E, Pierson JM, Bradshaw (1992) Initiation and execution of movement sequences in those suffering from and at-risk of developing Huntington's disease. J Clin Exp Neuropsychol 14:179-192.
22. Brown LL (1992) Somatotopic organization in rat striatum: evidence for a combinatorial map. Proc Natl Acad Sci USA 15:7403-7407.
23. Brown LL, Feldman SM, Divac I, Hand PJ, Lidsky TI (1995) A distributed network of context dependent functional units in the rat neostriatum. In: The basal ganglia IV (Percheron G, McKenzie JS, Feger J, eds), pp 215-228. New York: Plenum.
24. Brown RG, Jahanshahi M, Marsden CD (1993) The execution of bimanual movements in patient with Parkinson's, Huntington's and cerebellar disease. J Neurol Neurosurg Psychiatry 56:295-297.
25. Butters N, Wolfe J, Martone M, Granholm E, Cermack LS (1985) Memory disorders associated with Huntington's disease: verbal recall, verbal recognition, procedural memory. Neuropsychology 23:729-743.
26. Campbell KM, Dill RE (1974) Trunk rigidity and limb hypotonia produced in squirrel monkeys by direct cholinergic stimulation of the globus pallidus. Exp Neurol 42:555-565.
27. Carelli RM, West MO (1991) Representation of the body by single neurons in the dorsolateral striatum of the awake, unrestrained rat. J Comp Neurol 309:231-249.
28. Colonnese MT, Stallman EL, Berridge KC (1996) Ontogeny of action syntax in altricial and precocial rodents: grooming sequences by rat and guinea pig pups. Behaviour, in press.
29. Cools AR (1980) Role of the neostriatal dopaminergic activity in sequencing and selecting behavioural strategies: facilitation of processes involved in selecting the best strategy in a stressful situation. Behav Brain Res 1:361-378.
30. Cools AR (1985) Brain and behavior: hierarchy of feedback systems and control of input. In: Perspectives in ethology (Bateson PPG, Klopfer PH, eds), pp 109-168. New York: Plenum.
31. Cummings JL, Frankel M (1985) Gilles de la Tourette syndrome and the neurological basis of obsessions and compulsions. Biol Psychiatry 20:1117-1126.
32. Cromwell HC, Berridge KC (1990) Anterior lesions of the corpus striatum produce a disruption of stereotypic grooming sequences in the rat. Soc Neurosci Abstr. 16:233.
33. Cromwell HC, Berridge KC (1993) Where does damage produce enhanced aversion: the ventral pallidum/substantia innominata or lateral hypothalamus? Brain Res 624:1-10.
34. Cromwell HC, Berridge KC (1994) Mapping of globus pallidus and ventral pallidum lesions that produce hyperkinetic treading. Brain Res 668:16-29.
35. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281-285.
36. DeLong MR, Alexander GE, Georgopoulos AP, Crutcher MD, Mitchell SJ, Richardson RT (1984) Role of basal ganglia in limb movements. Hum Neurobiol 2:235-244.
37. Delong MR, Coyle JT (1979) Globus pallidus lesions in the monkey produced by kainic acid: histologic and behavioral effects. Appl Neurophysiol 42:95-97.
38. Denny-Brown D (1962) The basal ganglia and their relation to disorders of movement. London: Oxford UP.
39. Divac I (1972) Neostriatum and functions of prefrontal cortex. Acta Neurobiol Exp 32:461-477.
40. Divac I, Diemer NH (1980) Prefrontal system in the rat visualized by means of labeled deoxyglucose: further evidence for functional heterogeneity of the neostriatum. J Comp Neurol 190:1-13.
41. Evarts EV, Kimura M, Wurtz RH, Hikosaka O (1984) Behavioral correlates of activity in basal ganglia neurons. Trends Neurosci 56:447-453.
42. Fentress JC (1972) Development and patterning of movement sequences in inbred mice. In: The biology of behavior (Kiger J, ed), pp. 83-132. Corvallis: Oregon State University.
43. Fentress JC (1992) Emergence of pattern in the development of mammalian movement sequences. J Neurobiol 23:1529-1556.
44. Feve A, Fenelon G, Wallays C, Remy P, Guillard A (1993) Axial motor disturbances after hypoxic lesions of the globus pallidus. Mov Disord 8:321-326.
45. Flaherty AW, Graybiel AM (1991) Corticostriatal transformations in the primate somatosensory system: projections from physiologically mapped body-part representations. J Neurophysiol 66:1249-1263.
46. Flaherty AW, Graybiel AM (1993) Two input systems for body representations in the primate striatal matrix: experimental evidence in the squirrel monkey. J Neurosci 13:1120-1137.
47. Folstein S (1989) Huntington's disease: a disorder of families. Baltimore: The John Hopkins University.
48. Frankel M, Cummings JL, Robertson MM, Trimble MR, Hill MA, Benson DR (1986) Obsessions and compulsions in Gilles de la Tourette's syndrome. Neurology 36:378-382.
49. Gabrieli J (1995) Contribution of the basal ganglia to skill learning and working memory in humans. In: Models of information processing in the basal ganglia (Houl JA, Davis JL, Beiser DB, eds), pp 277-294. Cambridge: MIT.
50. Gardiner TW, Kitai ST (1992) Single-unit activity in the globus pallidus and neostriatum of the rat during performance of a trained head movement. Exp Brain Res 88:517-530.
51. Georgiou N, Bradshaw JL, Iansek R, Phillips JG, Mattingley JB, Bradshaw JA (1994) Reduction in external cues and movement sequencing in Parkinson's disease. J Neurol Neurosurg Psychiatry 57:368-370.
52. Georgiou N, Bradshaw JL, Phillips JG, Bradshaw JA, Chiu E (1995) Advance information and movement sequencing in Gilles de la Tourette's syndrome. J Neurol Neurosurg Psychiatry 58:184-191.
53. Georgiou N, Iansek R, Bradshaw JL, Phillips JG, Mattingley JB, Bradshaw JA (1993) An evaluation of the role of internal cues in the pathogenesis of Parkinsonian hypokinesia. Brain 116:1575-1587.
54. Gerfen CR, Staines WA, Arbuthnott GW, Fibiger HC (1982) Crossed connections of the substantia nigra in the rat. J Comp Neurol 207:283-303.
55. Graybiel AM, Kimura M (1995) Adaptive neural networks in the basal ganglia. In: Models of information processing in the basal ganglia (Houk JC, Davis JL, Beiser DG, eds), pp 103-116. Cambridge: MIT.
56. Graybiel AM, Ragsdale Jr CW (1978) Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining. Proc Natl Acad Sci USA 75:5723-5726.
57. Graybiel AM, Aosaki T, Flaherty AW, Kimura M (1994) The basal ganglia and adaptive motor control. Science 265:1826-1831.
58. Grill HJ, Norgren R (1978) Neurological tests and behavioral deficits in chronic thalamic and chronic decerebrate rats. Brain Res 143:299-312.
59. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Moller A, Nielsen K, Nyengaard JR, Pakkenberg B (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881.
60. Haber SN, Groenewegen HJ, Grove EA, Nauta WJ (1985) Efferent connections of the ventral pallidum: evidence of a dual striato pallidofugal pathway. J Comp Neurol 235:322-335.
61. Haber SN, Kowall NW, Vonsattel JP, Bird ED, Richardson Jr EP (1986) Gilles de la Tourette's syndrome. A postmortem neuropathological and immunohistochemical study. J Neurol Sci 75:225-241.
62. Haber SN, Lynd-Balta E, Mitchell SJ (1993) The organization of the descending ventral pallidal projections in the monkey. J Comp Neurol 329:111-128.
63. Hali S, Schallert T (1988) Striatal dopamine and the interface between orienting and ingestive functions. Physiol Behav 44:469-471.
64. Harrington DL, Haaland KA (1991) Sequencing in Parkinson's disease. Brain 114:99-115.
65. Hazrati LN, Parent A (1992) The striatopallidal projection displays a high degree of anatomical specificity in the primate. Brain Res 592.213-227.
66. Hedreen JC, Folstein SE (1995) Early loss of neostriatal striosome neurons in Huntington's disease. J Neuropathol Exp Neurol 54:105-120.
67. Heindel WC, Salmon DP, Shults CW, Walicke PA, Butters N (1989) Neuropsychological evidence for multiple implicit memory systems: a comparison of Alzheimer's, Huntington's, and Parkinson's disease patients. J Neurosci 9:582-587.
68. Hoover JE, Strick PL (1993) Multiple output channels in the basal ganglia. Science 259:819-821.
69. Iversen LL (1979) The chemistry of the brain. Sci Am 241:134-149.
70. Jackson S, Houghton G (1995) Sensorimotor selection and the basal ganglia. In: Models of information processing in the basal ganglia (Houk JC, Davis JL, Beiser DG, eds), pp 337-368. Cambridge: MIT.
71. Jaspers RMA, de Vries TJ, Cools AR (1990) Enhancement in switching motor patterns following local application of the glutamate agonist AMPA into the cat caudate nucleus. Behav Brain Res 37:237-246.
72. Kelley AE, Domesick VB, Nauta WJ (1982) The amygdalostriatal projection in the rat: an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7:615-630.
73. Kermadi I, Joseph JP (1995) Activity in the caudate nucleus of monkey during spatial sequencing. J Neurophysiol 74:911-933.
74. Kermadi I, Jurquet Y, Arzi M, Joseph JP (1993) Neural activity in the caudate nucleus of monkeys during spatial sequencing. Exp Brain Res 94:352-356.
75. Kimura M, Aosaki T, Hu Y, Ishida A, Watanabe K (1992) Activity of primate putamen neurons is selective to the mode of voluntary movement: visually guided, self-initiated, or memory guided. Exp Brain Res 89:473-477.
76. Labuszewski T, Lockwood R, McManus R, Edelstein FE, Lidsky TI (1981) Role of postural deficits in oro-ingestive problems caused by globus pallidus lesions. Exp Neurol 74:93-110.
77. Lashley KS (1951) The problem of serial order in behavior. In: Cerebral mechanisms of behavior (Jefferies LA, ed), pp 112-136. New York: Wiley.
78. Lasiter PS, Garcia J (1984) A methoxyfturane delivery system for stereotaxic surgery. Brain Res Bull 13:457-460.
79. Levitt DA, Teitelbaum P (1975) Somnolence, akinesia and sensory activation of motivated behavior in the lateral hypothalamic syndrome. Proc Natl Acad Sci 72:2819-2823.
80. Lidsky TI, Manetto C, Schneider JS (1985) A consideration of sensory factors involved in motor functions of the basal ganglia. Brain Res 356:133-146.
81. Lieberman P, Kako E, Friedman J, Tajchman G, Feldman LS, Jiminez EB (1992) Speech production, syntax comprehension, and cognitive deficits in Parkinson's disease. Brain Lang 43:169-189.
82. Luxenberg JS, Swedo SE, Flament MF, Friedland RP, Rapoport J, Rapoport SI 1988 Neuroanatomical abnormalities in obsessive-compulsive disorder detected with quantitative x-ray computed tomography. Biol Psychiatry 145:1089-1093.
83. Mansbach RS, Geyer MA, Braff DL (1988) Dopaminergic stimulation disrupts sensorimotor gating in the rat. Psychopharmacology 94:507-514.
84. Marsden CD (1982) The mysterious motor function of the basal ganglia. Neurology 32:524-532.
85. Marsden CD (1984) Which motor disorder in Parkinson's disease indicates the true motor function of the basal ganglia? In: Functions of the basal ganglia (Evered D, O'Conner M, eds), pp 225-237. London: Pitman.
86. Marsden CD (1992) Dopamine and basal ganglia disorders in humans. Semin Neurosci 4:171-178.
87. McGeorge AJ, Faull RL (1989) The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29:503-537.
88. Mittler T, Cho J, Peoples LL, West MO (1994) Representation of the body in the lateral striatum of the freely moving rat: single neurons related to licking. Exp Brain Res 98:163-167.
89. Mogenson GJ, Nielsen MA (1983) Evidence that an accumbens to subpallidal GABAergic projection contributes to locomotor activity. Brain Res Bull 11:309-314.
90. Mogenson GJ, Yang CR (1991) The contribution of basal forebrain to limbic-motor integration and the mediation of motivation to action. Adv Exp Med Biol 295:267-290.
91. Montgomery EB, Buchholz SR (1991) The striatum and motor cortex in motor initiation and execution. Brain Res 549:222-229.
92. Mufson EJ, Brandabur MM (1994) Sparing of NADPH-diaphorase striatal neurons in Parkinson's and Alzheimer's diseases. NeuroReport 5:705-708.
93. Nakamura S, Muramatsu S, Yoshida M (1990) Role of the basal ganglia in manifestation of rhythmical jaw movement in rats. Brain Res 535:335-338.
94. Nauta WJH (1989) Reciprocal links of the corpus striatum with the cerebral cortex and the limbic system: a common substrate for movement and thought? In: Neurology and psychiatry: a meeting of the minds (Mueller, ed), pp 43-63. Basel: Karger.
95. Norton S (1976) Hyperactive behavior after lesions of the globus pallidus. Brain Res Bull 1:193-202.
96. Oepen G, Mohr U, Willmes K, Thoden U (1985) Huntington's disease: visuomotor disturbances in patients and offspring. J Neurol Neurosurg Psychiatry 48:426-433.
97. Owen AM, Leigh JM (1992) Frontostriatal cognitive deficits at different stages of Parkinson's disease. Brain 115:1727-1751.
98. Parent A (1986) Comparative neurobiology of the basal ganglia. Wiley series in neurobiology (Northcutt RG, ed). New York: Wiley.
99. Parent A, Decarries L, Beaudet A (1981) Organization of ascending serotonin systems in the rat brain. A radiographic study after intraventricular administration of 3H-5-hydroxy-tryptamine. Neuroscience 6:115-138.
100. Paxinos G, C Watson (1982) The rat brain in stereotaxic coordinates. New York: Academic.
101. Pellis SM, Castaneda E, Mckenna MM, Tran-Nguyen LTL, Whishaw IQ (1993) The role of the striatum in organizing sequences of play fighting in neonatally dopamine-depleted rats. Neurosci Lett 158:13-15.
102. Pierce RC, Rebec GV (1995) Iontophoresis in the neostriatum of awake, unrestrained rats: differential effects of dopamine, glutamate, and ascorbate on motor-and nonmotor-related neurons. Neuroscience 67:313-324.
103. Pisa M (1988) Motor functions of the striatum in the rat: critical role of the lateral region in tongue and forelimb reaching. Neuroscience 24:453-463.
104. Rajakumar N, Elisevich K, Flumerfelt BA (1993) Compartmental origin of the striato-entopeduncular projection in the rat. J Comp Neurol 331:286-296.
105. Rapoport J (1991) Recent advances in obsessive-compulsive disorder. Neuropsychopharmacology 5:1-20.
106. Rapoport J, Wise SP (1988) Obsessive-compulsive disorder: evidence for basal ganglia dysfunction. Psychopharmacol Bull 20:380-384.
107. Resnick SM (1992) Positron emission tomography in psychiatric illness. Curr Dir Psychol Sci 1:92-98.
108. Sabol KE, Neill DB, Wages SA, Church WH, Justice JB (1985) Dopamine depletion in a striatal subregion disrupts performance of a skilled motor task in the rat. Brain Res 335:33-43.
109. Sachs BD (1988) The development of grooming and its expression in adult animals. Ann NY Acad Sci 525:1-17.
110. Sadikot AF, Parent A, Smith Y, Bolam JP (1992) Efferent connections of the centromedian and parafiscular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity. J Comp Neurol 320:228-242.
111. Schallert T, Hall S (1988) "Disengage" sensorimotor deficit following apparent recovery from unilateral dopamine depletion. Behav Brain Res 30:15-24.
112. Schneider JS, Lidsky TI (1981) Processing of somatosensory information in striatum of behaving cats. J Neurophysiol 45:841-851.
113. Schneider JS, Olazabal UE (1984) Behaviorally specific limb use deficits following globus pallidus lesions in rats. Brain Res 308:341-346.
114. Schultz W, Apicella P, Ljungberg T, Romo R (1995) Activity of monkey striatal and dopamine neurons during the performance of delayed response tasks. In: The basal ganglia IV (Percheron G, Mckenzie JS, Feger J, eds), pp 305-316. New York: Plenum.
115. Selemon LD, Goldman-Rakic PS (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci 5:776-794.
116. Sprengelmeyer R, Canavan AGM, Lange HW, Homberg V (1995) Associative learning in degenerative neostriatal disorders: contrasts in explicit and implicit remembering between Parkinson's and Huntington's diseases. Mov Disord 10:51-65.
117. Staines WA, Atmadja S, Fibiger HC (1981) Demonstration of pallidostriatal pathway by retrograde transport of HRP-labeled lectin. Brain Res 206:446-450.
118. Stelmach GE, Worringham CJ, Strand EA (1987) The programming and execution of movement sequences in Parkinson's disease. Int J Neurosci 36:55-65.
119. Trimble M (1989) Psychopathology and movement disorders: a new perspective on the Gilles de la Tourette syndrome. J Neurol Neurosurg Psychiatry 52[Suppl]:90-95.
120. Van den Brecken JH, Cools AR (1982) Evidence for a role of the caudate nucleus in the sequential organization of behavior. Behav Brain Res 4:319-327.
121. Weiner SI (1993) Spatial and behavioral correlates of striatal neurons in rats performing a self-initiated navigation task. J Neurosci 13:3802-3817.
122. West MO, Carelli RE, Pomerantz M, Cohen SM, Gardiner JP, Chapin JK, Woodward DJ (1990) A region in the dorsolateral striatum of the rat exhibiting single-unit correlations with specific locomotor limb movements. J Neurophysiol 64:1233-1246.
123. Whishaw IQ, O'Conner WT, Dunnett SB (1986) The contributions of motor cortex, nigrostriatal dopamine and caudate putamen to skilled forelimb use in the rat. Brain 109:805-843.
124. Willingham DB, Koroshetz W (1993) Evidence for dissociable motor skills in Huntington's disease patients. Psychobiology 21:173-182.
125. Wilson SAK (1914) An experimental research into the anatomy and physiology of the corpus striatum. Brain 36:427-492.