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Substantia nigra pars reticulata neurons code initiation of a serial pattern: implications for natural action sequences and sequential disorders

dc.contributor.authorMeyer-Luehmann, Melanieen_US
dc.contributor.authorThompson, Jeffrey F.en_US
dc.contributor.authorBerridge, Kent C.en_US
dc.contributor.authorAldridge, J. Wayneen_US
dc.date.accessioned2010-06-01T18:35:35Z
dc.date.available2010-06-01T18:35:35Z
dc.date.issued2002-10en_US
dc.identifier.citationMeyer-Luehmann, Melanie; Thompson, Jeffrey F.; Berridge, Kent C.; Aldridge, J. Wayne (2002). "Substantia nigra pars reticulata neurons code initiation of a serial pattern: implications for natural action sequences and sequential disorders." European Journal of Neuroscience 16(8): 1599-1608. <http://hdl.handle.net/2027.42/71795>en_US
dc.identifier.issn0953-816Xen_US
dc.identifier.issn1460-9568en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/71795
dc.identifier.urihttp://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=12405974&dopt=citationen_US
dc.description.abstractSequences of movements are initiated abnormally in neurological disorders involving basal ganglia dysfunction, such as Parkinson's disease or Tourette's syndrome. The substantia nigra pars reticulata (SNpr) is one of the two primary output structures of the basal ganglia. However, little is known about how substantia nigra mediates the initiation of normal movement sequences. We studied its role in coding initiation of a sequentially stereotyped but natural movement sequence by recording neuronal activity in SNpr during behavioural performance of ‘syntactic grooming chains’. These are rule-governed sequences of up to 25 grooming movements emitted in four predictable (syntactic) phases, which occur spontaneously during grooming behaviour by rats and other rodents. Our results show that neuronal activation in central SNpr codes the onset of this entire rule-governed sequential pattern of grooming actions, not elemental grooming movements. We conclude that the context of sequential pattern may be more important than the elemental motor parameters in determining SNpr neuronal activation.en_US
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dc.format.extent3109 bytes
dc.format.mimetypeapplication/pdf
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dc.publisherBlackwell Science Ltden_US
dc.rightsFederation of European Neuroscience Societiesen_US
dc.subject.otherBasal Gangliaen_US
dc.subject.otherDopamineen_US
dc.subject.otherFixed Action Patternen_US
dc.subject.otherGroomingen_US
dc.subject.otherHuntington's Diseaseen_US
dc.subject.otherMovement Sequencesen_US
dc.subject.otherMovementen_US
dc.subject.otherNeuroethologyen_US
dc.subject.otherNeuronal Activityen_US
dc.subject.otherObsessive–Compulsive Disorderen_US
dc.subject.otherParkinson's Diseaseen_US
dc.subject.otherRaten_US
dc.subject.otherSerial Orderen_US
dc.subject.otherSyntaxen_US
dc.subject.otherTourette's Syndromeen_US
dc.titleSubstantia nigra pars reticulata neurons code initiation of a serial pattern: implications for natural action sequences and sequential disordersen_US
dc.typeArticleen_US
dc.subject.hlbsecondlevelNeurosciencesen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumDepartment of Psychology, University of Michigan, Ann Arbor, MI 48109–1109, USAen_US
dc.contributor.affiliationumDepartment of Neurology, University of Michigan, Ann Arbor, MI 48109–0489, USAen_US
dc.contributor.affiliationotherDepartment of Neuropathology, University of Basel, Switzerlanden_US
dc.contributor.affiliationotherPhysiological Science, 4117 LSB, University of California, Los Angeles, Los Angeles, CA 90095–1606, USAen_US
dc.identifier.pmid12405974en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/71795/1/j.1460-9568.2002.02210.x.pdf
dc.identifier.doi10.1046/j.1460-9568.2002.02210.xen_US
dc.identifier.sourceEuropean Journal of Neuroscienceen_US
dc.identifier.citedreferenceAlbin, R. L., Young, A. B. & Penney, J. B. ( 1989 ) The functional anatomy of basal ganglia disorders. Trends Neurosci., 12, 366 – 375.en_US
dc.identifier.citedreferenceAldridge, J. W. & Berridge, K. C. ( 1998 ) Coding of serial order by neostriatal neurons: a ‘natural action’ approach to movement sequence. J. Neurosci., 18, 2777 – 2787.en_US
dc.identifier.citedreferenceAldridge, J. W., Berridge, K. C., Herman, M. & Zimmer, L. ( 1993 ) Neuronal coding of serial order: syntax of grooming in the neostriatum. Psychol. Sci., 4, 391 – 395.en_US
dc.identifier.citedreferenceBeiser, D. G. & Houk, J. C. ( 1998 ) Model of cortical-basal ganglionic processing: encoding the serial order of sensory events. J. Neurophysiol., 79, 3168 – 3188.en_US
dc.identifier.citedreferenceBerns, G. S. & Sejnowski, T. J. ( 1998 ) A computational model of how the basal ganglia produce sequences. J. Cogn. Neurosci., 10, 108 – 121.en_US
dc.identifier.citedreferenceBerridge, K. C. & Aldridge, J. W. ( 2000a ) Super-stereotypy I: Enhancement of a complex movement sequence by systemic dopamine D1 agonists. Synapse, 37, 194 – 204.en_US
dc.identifier.citedreferenceBerridge, K. C. & Aldridge, J. W. ( 2000b ) Super-stereotypy II: Enhancement of a complex movement sequence by intraventricular dopamine D1 agonists. Synapse, 37, 205 – 215.en_US
dc.identifier.citedreferenceBerridge, K. C., Fentress, J. C. & Parr, H. ( 1987 ) Natural syntax rules control action sequence of rats. Behav. Brain Res., 23, 59 – 68.en_US
dc.identifier.citedreferenceBerridge, K. C. & Whishaw, I. Q. ( 1992 ) Cortex, striatum, and cerebellum: control of serial order in a grooming sequence. Exp. Brain. Res., 90, 275 – 290.en_US
dc.identifier.citedreferenceChurchward, P. R., Butler, E. G., Finkelstein, D. I., Aumann, T. D., Sudbury, A., Horne &, M. K. ( 1997 ) A comparison of methods used to detect changes in neuronal discharge patterns. J. Neurosci. Meth, 76, 203 – 210.en_US
dc.identifier.citedreferenceCromwell, H. C. & Berridge, K. C. ( 1996 ) Implementation of action sequences by a neostriatal site: a lesion mapping study of grooming syntax. J. Neurosci., 16, 3444 – 3458.en_US
dc.identifier.citedreferenceCurra, A., Berardelli, A., Agostino, R., Modugno, N., Puorger, C. C., Accornero, N. & Manfredi, M. ( 1997 ) Performance of sequential arm movements with and without advance knowledge of motor pathways in Parkinson's disease. Mov. Disord., 12, 646 – 654.en_US
dc.identifier.citedreferenceDeLong, M. R., Crutcher, M. D. & Georgopoulos, A. P. ( 1983 ) Relations between movement and single cell discharge in the substantia nigra of the behaving monkey. J. Neurosci., 3, 1599 – 1606.en_US
dc.identifier.citedreferenceFujimoto, K. & Kita, H. ( 1993 ) Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res., 609, 185 – 192.en_US
dc.identifier.citedreferenceGulley, J. M., Kuwajima, M., Mayhill, E. & Rebec, G. V. ( 1999 ) Behavior-related changes in the activity of substantia nigra pars reticulata neurons in freely moving rats. Brain Res., 845, 68 – 76.en_US
dc.identifier.citedreferenceHaber, S. N., Fudge, J. L. & McFarland, N. R. ( 2000 ) Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J. Neurosci., 20, 2369 – 2382.en_US
dc.identifier.citedreferenceHarrington, D. L. & Haaland, K. Y. ( 1991 ) Sequencing in Parkinson's disease – abnormalities in programming and controlling movement. Brain, 114, 99 – 115.en_US
dc.identifier.citedreferenceHo, A. K., Bradshaw, J. L., Cunnington, R., Phillips, J. G. & Iansek, R. ( 1998 ) Sequence heterogeneity in Parkinsonian speech. Brain Language, 64, 122 – 145.en_US
dc.identifier.citedreferenceJaeger, D., Gilman, S. & Aldridge, J. W. ( 1990 ) A multiwire microelectrode for single unit recording in deep brain structures. J. Neurosci. Meth, 32, 143 – 148.en_US
dc.identifier.citedreferenceKermadi, I. & Joseph, J. P. ( 1995 ) Activity in the caudate nucleus of monkey during spatial sequencing. J. Neurophysiol., 74, 911 – 933.en_US
dc.identifier.citedreferenceKitai, S. T. & Deniau, J. M. ( 1981 ) Cortical inputs to the subthalamus: intracellular analysis. Brain Res., 214, 411 – 415.en_US
dc.identifier.citedreferenceKolomiets, B. P., Deniau, J. M., Mailly, P., Menetrey, A., Glowinski, J. & Thierry, A. M. ( 2001 ) Segregation and convergence of information flow through the cortico-subthalamic pathways. J. Neurosci., 21, 5764 – 5772.en_US
dc.identifier.citedreferenceLang, A. E., Consky, E. & Sandor, P. ( 1993 ) ‘Signing tics’– insights into the pathophysiology of symptoms in Tourette's syndrome. Ann. Neurol., 33, 212 – 215.en_US
dc.identifier.citedreferenceLashley, K. S. ( 1951 ) The problem of serial order in behavior. In Jeffress, L. A. (ed.), Cerebral Mechanisms in Behavior. Wiley, New York, pp. 112 – 146.en_US
dc.identifier.citedreferenceLevy, R., Hazrati, L. N., Herrero, M. T., Vila, M., Hassani, O. K., Mouroux, M., Ruberg, M., Asensi, H., Agid, Y., Feger, J., Obeso, J. A., Parent, A. & Hirsch, E. C. ( 1997 ) Re-evaluation of the functional anatomy of the basal ganglia in normal and parkinsonian states. Neuroscience, 76, 335 – 343.en_US
dc.identifier.citedreferenceLieberman, P. ( 2001 ) Human language and our reptilian brain. The subcortical bases of speech, syntax, and thought. Perspect. Biol. Med., 44, 32 – 51.en_US
dc.identifier.citedreferenceLieberman, P., Kako, E., Friedman, J., Tajchman, G., Feldman, L. S. & Jiminez, E. B. ( 1992 ) Speech production, syntax comprehension, and cognitive deficits in Parkinson's disease. Brain Language, 43, 169 – 189.en_US
dc.identifier.citedreferenceLimousin, P., Pollak, P., Benazzouz, A., Hoffmann, D., Le Bas, J. F., Broussolle, E., Perret, J. E. & Benabid, A. L. ( 1995 ) Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet, 345, 91 – 95.en_US
dc.identifier.citedreferenceMahon, S., Delord, B., Deniau, J. M. & Charpier, S. ( 2000 ) Intrinsic properties of rat striatal output neurones and time-dependent facilitation of cortical inputs in vivo. J. Physiol. (Lond. ), 527, 345 – 354.en_US
dc.identifier.citedreferenceMarsden, C. D. & Obeso, J. A. ( 1994 ) The functions of the basal ganglia and the paradox of stereotaxic surgery in Parkinson's disease. Brain, 117, 877 – 897.en_US
dc.identifier.citedreferenceMartin, K. E., Phillips, J. G., Iansek, R. & Bradshaw, J. L. ( 1994 ) Inaccuracy and instability of sequential movements in Parkinson's disease. Exp. Brain Res., 102, 131 – 140.en_US
dc.identifier.citedreferenceMatsumoto, N., Hanakawa, T., Maki, S., Graybiel, A. M. & Kimura, M. ( 1999 ) Nigrostriatal dopamine system in learning to perform sequential motor tasks in a predictive manner. J. Neurophysiol., 82, 978 – 998.en_US
dc.identifier.citedreferenceMink, J. W. ( 1996 ) The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol., 50, 381 – 425.en_US
dc.identifier.citedreferenceMushiake, H. & Strick, P. L. ( 1995 ) Pallidal neuron activity during sequential arm movements. J. Neurophysiol., 74, 2754 – 2758.en_US
dc.identifier.citedreferenceNakanishi, H., Kita, H. & Kitai, S. T. ( 1987 ) Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res., 437, 45 – 55.en_US
dc.identifier.citedreferenceO'Quinn, A. N. & Thompson, R. J. Jr ( 1980 ) Tourette's syndrome: an expanded view. Pediatrics, 66, 420 – 424.en_US
dc.identifier.citedreferenceRapoport, J. L. & Wise, S. P. ( 1988 ) Obsessive–compulsive disorder: evidence for basal ganglia dysfunction. Psychopharmacol. Bull., 24, 380 – 384.en_US
dc.identifier.citedreferenceRedgrave, P., Prescott, T. J. & Gurney, K. ( 1999 ) The basal ganglia: a vertebrate solution to the selection problem? Neuroscience, 89, 1009 – 1023.en_US
dc.identifier.citedreferenceSchultz, W. ( 1986a ) Activity of pars reticulata neurons of monkey substantia nigra in relation to motor, sensory, and complex events. J. Neurophysiol., 55, 660 – 677.en_US
dc.identifier.citedreferenceSchultz, W. ( 1986b ) Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey. J. Neurophysiol., 56, 1439 – 1461.en_US
dc.identifier.citedreferenceSchultz, W. ( 1998 ) Predictive reward signal of dopamine neurons. J. Neurophysiol., 80, 1 – 27.en_US
dc.identifier.citedreferenceSmith, Y., Bevan, M. D., Shink, E. & Bolam, J. P. ( 1998 ) Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience, 86, 353 – 387.en_US
dc.identifier.citedreferenceSwanson, L. W. ( 1992 ) Brain Maps: Structure of the Rat Brain. Elsevier, Amsterdam.en_US
dc.identifier.citedreferenceToates, F. ( 1990 ) Obsessional Thoughts and Behaviour. Thorsons Publishing Group, Wellingborough.en_US
dc.identifier.citedreferenceVan Spaendonck, K. P., Horstink, M. W. I. M., Buytenhuijs, E. L., Cools, A. R. & Berger, H. J. C. ( 1996 ) Executive functions and disease characteristics in Parkinson's disease. Neuropsychologia, 34, 617 – 626.en_US
dc.identifier.citedreferenceWaddington, J. L., Deveney, A. M., Clifford, J., Tighe, O., Croke, D. T., Sibley, D. R. & Drago, J. ( 1998 ) Behavioral analysis of multiple D1-like dopamine receptor subtypes: new agents and studies in transgenic mice with D1A receptor knockout. Adv. Pharmacol. (New York), 42, 514 – 517.en_US
dc.identifier.citedreferenceWestwater, H., McDowall, J., Siegert, R., Mossman, S. & Abernethy, D. ( 1998 ) Implicit learning in Parkinson's disease: evidence from a verbal version of the serial reaction time task. J. Clin. Exp. Neuropsychol., 20, 413 – 418.en_US
dc.identifier.citedreferenceWichmann, T., Bergman, H., Starr, P. A., Subramanian, T., Watts, R. L. & DeLong, M. R. ( 1999 ) Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates. Exp. Brain Res., 125, 397 – 409.en_US
dc.identifier.citedreferenceWichmann, T. & DeLong, M. R. ( 1996 ) Functional and pathophysiological models of the basal ganglia. Curr. Opin. Neurobiol., 6, 751 – 758.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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