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Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex

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Abstract

Based on behavioral procedures aimed at measuring working or data-based memory for spatial location, response, and visual object information, it is shown that there is a triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex in mediating spatial location, response, and visual object information, respectively. The hippocampus appears to subserve only spatial location, the caudate nucleus only response, and the extrastriate visual cortex only visual object information. The results support the neurobiological foundation of the attribute memory model.

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]References

  • Aggleton JP, Blindt HS, Rawlins JNP (1989) Effects of amygdaloid and amygdaloid-hippocampal lesions on object recognition and spatial working memory in rats. Behav Neurosci 103:962–974

    Google Scholar 

  • Cave CB, Squire LR (1991) Equivalent impairment of spatial and nonspatial memory following damage to the human hippocampus. Hippocampus 1:329–340

    Google Scholar 

  • Chiba AA, Kesner RP, Matsuo F, Heilbrun PM (1990) A dissociation between verbal and spatial memory following unilateral temporal lobectomy. Soc Neurosci Abstr 16:286

    Google Scholar 

  • Cook D, Kesner RP (1988) Caudate nucleus and memory for egocentric localization. Behav Neural Biol 49:332–343

    Google Scholar 

  • Cornwell P, Warren JM (1982) Evaluation of visual performance in cats with posterior extrastriate lesions. In: Ingle WM, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT, Cambridge, Mass., pp 751–771

    Google Scholar 

  • Farah MJ (1990) Visual agnosia. MIT, Cambridge, Mass.

    Google Scholar 

  • Goodale MA, Dale RHI (1981) Radial-maze performance in the rat following lesions of posterior neocortex. Behav Brain Res 3:273–288

    Google Scholar 

  • Hunt MA, Kesner RP, DeSpain MJ (1986) The role of the hippocampus and the septo-hippocampal pathway on working (data-based) and reference (expectancy-based) memory in the rat. Soc Neurosci Abstr 12:744

    Google Scholar 

  • Hopkins RO, Kesner RP (1990) Data based (episodic) memory for motor responses in hypoxic patients. Soc Neurosci Abstr 16(I): 286

    Google Scholar 

  • Jackson-Smith P, Kesner RP, Chiba AA (1991) Continuous recognition of 3-dimensional objects in rats with hippocampal and medial prefrontal cortex lesions. Soc Neurosci Abstr 17:131

    Google Scholar 

  • Jagielo JA, Nonneman AJ, Isaac WL, Jackson-Smith PA (1990) Hippocampal lesions impair rats' performance of a nonspatial matching-to-sample task. Psychobiology 18:55–62

    Google Scholar 

  • Jones B, Mishkin M (1972) Limbic lesions and the problem of stimulus-reinforcement associations. Exp Neurol 36:362–377

    Article  CAS  PubMed  Google Scholar 

  • Kesner RP (1990) Learning and memory in rats with an emphasis on the role of the hippocampal formation. In: Kesner RP, Olton DS (eds), Neurobiology of Comparative Cognition, Erlbaum, Hillsdale, pp 179–204

    Google Scholar 

  • Kesner RP (1991) Neurobiological views of memory. In: Martinez JS, Kesner RP (eds) Eearning and memory, 2nd edn. Academic, New York, pp 499–547

    Google Scholar 

  • Kesner RP (1992) Learning and memory in rats with an emphasis on the role of the amygdala. In: Aggleton J (ed) The amygdala. Wiley, New York, 170–203

    Google Scholar 

  • Kesner RP, DiMattia BV (1987) Neurobiology of an attribute model of memory. In: Morrison AR, Epstein AN (eds) Progress in psychobiology and physiological psychology. Academic, New York, pp 207–277

    Google Scholar 

  • Kesner RP, Crutcher KA, Beers D (1988) Serial position curves for item (spatial) information: role of the dorsal hippocampus and medial septum. Brain Res 454:219–226

    Google Scholar 

  • Kesner RP, Hopkins RO, Chiba AA (1992) Learning and memory in humans with an emphasis on the role of the hippocampus. In: Squire L, Butters N (eds) Neuropsychology of memory, 2nd edn. Guilford, New York, 106–121

    Google Scholar 

  • Kitsikis A, Angyan L, Buser P (1971) Basal ganglia unitary activity during a motor performance in monkeys. Physiol Behav 6:609–611

    Google Scholar 

  • Kubie JL, Ranck JB (1983) Sensory-behavioral correlates in individual hippocampal neurons in three situations: space and context. In: Seifert W (ed) Neurobiology of the hippocampus. Academic, New York, pp 433–447

    Google Scholar 

  • Leonard G, Milner B (1991) Contribution of the right frontal lobe to the encoding and recall of kinesthetic distance information. Neuropsychologia 29:47–58

    Google Scholar 

  • Levine DN (1982) Visual agnosia in monkey and in man. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT, Cambridge, Mass. pp 629–670

    Google Scholar 

  • Martin-Elkins CL, George P, Horel JA (1991) Retention deficits produced in monkeys with reversible cold lesions in the prestriate cortex. Behav Brain Res 32:219–230

    Google Scholar 

  • McDaniel WF, Wall TT (1988) Visuospatial functions in the rat following injuries to striate, peristriate, and parietal neocortical sites. Psychobiology 16:251–260

    Google Scholar 

  • McNaughton BL, Barnes CA, O'Keefe J (1983) The contributions of position, direction and velocity to single unit activity in the hippocampus of freely moving rats. Exp Brain Res 52:41–49

    CAS  PubMed  Google Scholar 

  • Mishkin M (1978) Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273:297–298

    Google Scholar 

  • Mumby DG, Wood ER, Pinel JPJ (1992) Object recognition memory is only mildly impaired in rats with lesions of the hippocampus and amygdala. Psychobiology 20:18–27

    Google Scholar 

  • Olton DS (1983) Memory functions and the hippocampus. In: Seifert W (ed) Neurobiology of the hippocampus. Academic, New York, pp 335–373

    Google Scholar 

  • Olton DS (1986) Hippocampal function and memory for temporal context. In: Isaacson RL, Pribram KH, (eds) The hippocampus, vol 4. Plenum, New York, pp 281–298

    Google Scholar 

  • Olton DS, Feustle WA (1981) Hippocampal function required for non-spatial working memory. Exp Brain Res 41:380–389

    Google Scholar 

  • Packard MG, Hirsh R, White N (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9:1465–1472

    CAS  PubMed  Google Scholar 

  • Parkinson JK, Murray EA, Mishkin M (1988) A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. J Neurosci 8:4159–4167

    Google Scholar 

  • Potegal M (1971) A note on spatial-motor deficits in patients with Huntington's disease: a test of a hypothesis. Neuropsychology 9:233–235

    Google Scholar 

  • Potegal M (1982) Vestibular and neostriatal contributions to spatial orientation. In: Potegal M (ed) Spatial abilities, development and physiological foundation. Academic, New York, pp 361–387

    Google Scholar 

  • Raffaele KC, Olton DS (1988) Hippocampal and amygdaloid involvement in working memory. Exp Brain Res 41:380–389

    Google Scholar 

  • Rawlins JNP, Lyford G, Seferiades A (1991) Does it still make sense to develop nonspatial theories of hippocampal function? Hippocampus 1:283–286

    Google Scholar 

  • Rolls ET, Thorpe SJ, Maddison SP (1983) Responses of striatal neurons in the behaving monkey. 1. Head of the caudate nucleus. Behav Brain Res 7:179–210

    Google Scholar 

  • Rolls ET, Miyashita Y, Cahusac, PMB, Kesner RP, Niki H, Feigenbaum J, Bach L (1989) Hippocampal neurons in the monkey with activity related to the place in which a stimulus is shown. J Neurosci 9:1835–1844

    CAS  PubMed  Google Scholar 

  • Rothblat LA, Kromer LF (1991) Object recognition memory in the rat: the role of the hippocampus. Behav Brain Res 42:25–32

    Google Scholar 

  • Schacter DL (1987) Implicit memory: history and current status. J Exp Psychol [Learn Mem Cogn] 13:501–508

    Google Scholar 

  • Smith ML, Milner B (1981) The role of the right hippocampus in the recall of spatial location. Neuropsychologia 19:781–793

    Google Scholar 

  • Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253:1380–1386

    Google Scholar 

  • Ungerleider LG, Mishkin M (1982) Two cortical visual systems. In: Ingle DJ, Goodale MA, Mansfield RJW (eds) Analysis of visual behavior. MIT, Cambridge, Mass., pp 549–586

    Google Scholar 

  • Wilburn MW, Kesner RP (1974) Effects of caudate nucleus stimulation upon initiation and performance of a complex motor task. Exp Neurol 45:61–71

    Google Scholar 

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Kesner, R.P., Bolland, B.L. & Dakis, M. Memory for spatial locations, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp Brain Res 93, 462–470 (1993). https://doi.org/10.1007/BF00229361

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