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Cortex, striatum and cerebellum: control of serial order in a grooming sequence

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Summary

Rats emit grooming actions in sequences that follow characteristic patterns of serial order. One of these patterns, a syntactic chain, has a particularly stereotyped order that recurs spontaneously during grooming thousands of times more often than could occur by chance. Previous studies have shown that performance of this sequence is impaired by excitotoxin lesions of the corpus striatum. In this study we examined whether the striatum is unique in its importance to this behavioral sequence or whether control of the sequence instead depends equally upon the cortex and cerebellum. In two experiments, a fine-grained behavioral analysis compared the effects of striatal ablation to the effects of motor cortex ablation, ablation of the entire neocortex, or ablation of the cerebellum. Cortical and cerebellar aspiration produced mere temporary deficits in grooming sequences, which appeared to reflect a general factor that was nonsequential in nature. Only striatal damage produced a permanent sequential deficit in the coordination of this syntactic grooming chain. We conclude that the striatum has a unique role in the control of behavioral serial order. This striatal role may be related to a number of sequential disorders observed in human diseases involving the striatum.

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References

  • Aldridge JW, Berridge KC, Herman M (1990) Single unit activity in the rat caudate-putamen during stereotypical grooming sequences. Neurosci Abstr 16: 233

    Google Scholar 

  • Aldridge JW, Gilman J, Dauth G (1990) Spontaneous neuronal unit activity in the primate basal ganglia and the effects of precentral cerebral cortical ablations. Brain Res 516: 46–56

    Google Scholar 

  • Barone P, Joseph JP (1989) Prefrontal cortex and spatial sequencing in macaque monkey. Exp Brain Res 78: 447–464

    Google Scholar 

  • Berntson GG, Jang JF, Ronca AE (1988) Brainstem systems and grooming behaviors. Ann New York Acad Sci 525: 350–362

    Google Scholar 

  • Berridge KC (1989a) Progressive degradation of serial grooming chains by descending decerebration. Behav Brain Res 33: 241–253

    Google Scholar 

  • 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

    Google Scholar 

  • Berridge KC (1990) Comparative fine structure of action: rules of form and sequence in the grooming patterns of six rodent species. Behavior 113: 1–2

    Google Scholar 

  • Berridge KC, Fentress JC (1986) Contextual control of trigeminal sensorimotor function. J Neurosci 9: 325–330

    Google Scholar 

  • Berridge KC, Fentress JC (1987a) Deafferentation does not disrupt natural rules of action syntax. Behav Brain Res 23: 69–76

    Google Scholar 

  • Berridge KC, Fentress JC (1987b) Disruption of natural grooming chains after striatopallidal lesions. Psychobiology 15: 336–342

    Google Scholar 

  • Brunner RS, Kornhuber HH, Seemüller E, Suger G, Wallesch C-W (1982) Basal ganglia participation in language pathology. Brain Language 16: 281–299

    Google Scholar 

  • Buchtel HA (1970) Visual-learning deficits following cerebellar damage in rats. J Comp Physiol Psychol 72: 296–305

    Google Scholar 

  • Cools, AR (1985) Brain and behavior: hierarchy of feedback systems and control of input. In: Bateson PPG, Klopfer PH (eds). Perspectives in ethology. Plenum, New York, 109–168

    Google Scholar 

  • Cromwell HC, Berridge KC (1990) Anterior lesions of the corpus striatum produce a disruption of stereotyped grooming sequences in the rat. Neurosci Abstr 16: 233

    Google Scholar 

  • Cummings JL, Frankel M (1985) Gilles de la Tourette syndrome and the neurological basis of obsessions and compulsions. Biol Psychiatr 20: 1117–1126

    Google Scholar 

  • Dichgans J (1984) Clinical symptoms of cerebellar dysfunction and their topodiagnostic significance. Human Neurobiol 2: 269–279

    Google Scholar 

  • Divac I, Oberg GE, Rosenkilde CE (1987) Patterned neural activity: implications for neurology and neuropharmacology. In: Schneider JS, Lidsky TI (eds). Basal ganglia and behavior: sensory aspects of motor fractioning. Huber, Toronto, pp 61–70

    Google Scholar 

  • Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212: 76–88

    Google Scholar 

  • Evarts EV, Wise SP (1984) Basal ganglia outputs and motor control. Ciba Found Sympos 107: 83–102

    Google Scholar 

  • Fentress JC (1983) Ethological models of hierarchy and patterning of species-specific behavior. In: Satinoff E, Teitelbaum P (eds). Handbook of behavioral neurobiology. Plenum, New York, pp 185–234

    Google Scholar 

  • Fentress JC, Stilwell F (1973) Grammar of a movement sequence in inbred mice. Nature (Lond) 244: 52–53

    Google Scholar 

  • Ferron J, Lefebvre L (1982) Comparative organization of grooming sequences in adult and young sciurid rodents. Behaviour 81: 110–127

    Google Scholar 

  • Gallistel CR (1980) The organization of action: a new synthesis. Erlbaum, Hillsdale NJ

    Google Scholar 

  • Golani I, Wolgin DL, Teitelbaum P (1982) A proposed natural geometry of recovery from akinesia in the lateral hypothalamic rat, Brain Res 164: 237–67

    Google Scholar 

  • Goldman-Rakic PS (1987) Circuity of primate prefrontal cortex and regulation of behavior by representational memory. Hand Physiol 5: 373–417

    Google Scholar 

  • Iversen SD, Mishkin M (1979) Behavior after neostriatal lesions in animals. In: Divac I, Oberg RGE (eds) The neostriatum. Pergamon, New York, 183–195

    Google Scholar 

  • Iversen SD, Mishkin M (1970) Perseverative interference in monkeys following selective lesions of the inferior prefrontal conexity. Exp Brain Res 11: 376–386

    CAS  PubMed  Google Scholar 

  • Kelley AE, Domesick VB, Nauta WJH (1982) The amygdalostriatal projection in the rat. An anatomical study by anterograde and retrograde tracing methods. Neuroscience 615–630

  • Kirk WT, Berntson GG, Hothersall D (1982) Effects of paleocerebellar lesions on DRL performance in the albino rat. J Comp Physiol Psychol 96: 348–360

    Google Scholar 

  • Kolb B (1984) Functions of the frontal cortex of the rat: A comparative review. Brain Res 8: 65–98

    Article  Google Scholar 

  • Kolb B & Milner B (1981) Performance of complex arm and facial movements after focal lesions. Neuropsychology 19: 505–514

    Google Scholar 

  • Kolb B, Whishaw IQ & Schallert T (1972) Behavior sequencing, sensory neglect, and bodyweight set point following orbital frontal lesions in rats. Physiol Behav 19: 93–102

    Google Scholar 

  • Kurata K, Wise SP (1988) Premotor and supplementary motor cortex in Rhesus monkeys: neuronal activity during externally — and internally — instructed motor tasks. Exp Brain Res 72: 237–284

    CAS  PubMed  Google Scholar 

  • Lashley KS (1951) The problem of serial order in behavior. In: Jeffress LA (eds) Cerebral mechanisms in behavior. Wiley, New York, pp 112–136

    Google Scholar 

  • Lashley KS, McCarthy DA (1926) The survival of the maze habit after cerebellar lesions. J Comp Psychol 6: 423–433

    Google Scholar 

  • Levitt DR, Teitelbaum P (1975) Somnolence, akinesia, and sensory activation of motivated behavior in the lateral hypothalamic syndrome. Proc Nat Acad Sci 72: 2819–2823

    Google Scholar 

  • Luxenberg JS, Swedo SE, Flament MF, Friedland RP, Rapoport JL, Rapoport SI (1988) Neuroanatomical abnormalities in obsessive-compulsive disorder detected with quantitative x-ray computed tomography. Am J Psychiatr 145: 1089–1093

    Google Scholar 

  • MacLean PD (1990) The Triune Brain in evolution: Role in Paleocerebral Functions. New York: Plenum

    Google Scholar 

  • Manetto C, Lidsky TI (1987) Influences of the basal ganglia on the medullary reticular formation. Neurosci Let 75: 278–282

    Google Scholar 

  • Marsden CD (1982) The mysterious motor function of the basal ganglia: The Robert Wartenberg lecture. Neurology 32: 514–539

    Google Scholar 

  • Nauta WJH, Domesick VB (1984) Afferent and efferent relationships of the basal ganglia. In: Evered D, O'Connor M (eds) Functions of the basal ganglia: Ciba Foundation Symposium. Pitman, London, 107:3–23

    Google Scholar 

  • Neafsey EJ (1990) The complete ratunculus: output organization of layer V of the cerebral cortex. In Kolb B, Tees RC (eds) The cerebral cortex of the rat. MIT, Cambridge, pp 197–212

    Google Scholar 

  • Neafsey EJ, Bold EL, Haas G, Hurley-Gius KM, Quirk G, Sievert CF, Terreberry RR (1986) The organization of the rat motor cortex: a microstimulation mapping study. Brain Res Rev 11: 77–96

    Google Scholar 

  • Passingham RE, Chen YC, Thaler D (1989) Supplementary motor cortex and self-initiated movement. In: Ito M (eds) Neural programming. Karger, Basel, pp 13–24

    Google Scholar 

  • Paxinos G, Watson G (1989) The rat brain in stereo toxic coordinates. Academic New York

    Google Scholar 

  • Pellegrino LJ, Altman J (1979) Effects of differential interference with postnatal cerebellar neurogenesis on motor performance, activity level, and maze learning of rats: a developmental study. J Comp Physiol Psychol 93: 1–33

    Google Scholar 

  • Pisa M, Cyr J (1990) Regionally selective roles of the rat's striatum in modality-specific discrimination learning and forelimb reaching. Behav Brain Res 37: 281–292

    Google Scholar 

  • Petrides M, Milner B (1982) Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man. Neuropsychology 20: 249–262

    Google Scholar 

  • Rapoport JL (1989) The boy who couldn't stop washing: the experience and treatment of obsessive-compulsive disorder. Penguin Books, New York

    Google Scholar 

  • Rapoport JL, Wise SP (1988) Obsessive-compulsive disorder: evidence for basal ganglia dysfunction. Psychopharm Bull 24: 380–384

    Google Scholar 

  • Richmond G, Sachs BD (1980) Grooming in Norway rats: the development and adult expression of a complex motor pattern. Behavior 75: 82–96

    Google Scholar 

  • Schneider JS, Kovelowski CJ 2d. (1990) Chronic exposure to low doses of MPTP. In: Cognitive deficits in motor asymptomatic monkeys. Brain Res 519, 122–128

    Google Scholar 

  • Shelton PA, Knopman DS (1991) Ideomotor apraxia in Huntington's disease. Arch Neurol 48: 35–41

    Google Scholar 

  • Thompson R (1974) Localization of the “maze memory system” in the white rat. Physiol Psychol 2: 1–17

    Google Scholar 

  • Vanderwolf CH, Kolb B, Cooley RK (1978) Behavior of the rat after removal at the neocortex and hippocampal dormation. J Comp Physiol 92: 156–175

    Google Scholar 

  • Van den Bercken JH, Cools AR (1982) Evidence for a role of the caudate nucleus in the sequential organization of behavior. Behav Brain Res 4: 319–327

    Google Scholar 

  • West O, Carelli RM, Pomerantz M, Cohen SM, Gardner JP, Chapin JK, Woodward DJ (199) A region in the dorsolateral striatum of the rat exhibiting single-unit correlations with specific locomotor limb movements. J Neurophysiol 64:1233–1246

    Google Scholar 

  • Whishaw IQ (1990) The decorticate rat. In: Kolb B, Tees RC (eds) The cerebral cortex of the rat. MIT, Cambridge, pp 239–268

    Google Scholar 

  • Whishaw IQ, Kolb M, Sutherland RJ (1983) The analysis of behavior in the laboratory rat. In: Robinson TE (eds) Behavioral approaches to brain research. Oxford University Press, New York, pp 141–211

    Google Scholar 

  • Whishaw IQ, O'Connor WT, Dunnett SB (1985) Disruption of central cholinergic systems in the rat by basal forebrain lesions or atropine: effects on feeding, sensorimotor behaviour, locomotor activity, and spatial navigation. Behav Brain Res 17: 103–115

    Google Scholar 

  • Whishaw IQ, Nonneman AJ, Kolb B (1981) Environmental constraints on motor abilities used in grooming, swimming, and eating by decorlicate rats. J Comp Physiol Psychol 95: 792–804

    Google Scholar 

  • Zilles K (1990) Anatomy of the neocortex: cytoarchitecture and my eloarchitecture. In: Kolb B, Tees RC (eds) The cerebral cortex of the rat. MIT, Cambridge, pp 77–112

    Google Scholar 

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Berridge, K.C., Whishaw, I.Q. Cortex, striatum and cerebellum: control of serial order in a grooming sequence. Exp Brain Res 90, 275–290 (1992). https://doi.org/10.1007/BF00227239

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  • DOI: https://doi.org/10.1007/BF00227239

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