Differential activation of the caudate nucleus in primates performing spatial and nonspatial working memory tasks
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The caudate nucleus is part of an anatomical network subserving functions associated with the dorsolateral prefrontal cortex (DLPFC). The aim of the present study was to investigate whether the metabolic activity in the striatum reflects specific changes in working memory tasks, which are known to be dependent on the DLPFC, and whether these changes reflect the topographic ordering of prefrontal connections within the striatum. Local cerebral glucose utilization (LCGU) rates were assessed in the striatum by the 14C-2-deoxyglucose method in monkeys that performed a spatial (delayed spatial alternation), a nonspatial (delayed object alternation) visual working memory task, or tasks that did not involve working memory, i.e., a visual pattern discrimination or sensorimotor paradigm. The results show a topographic segregation of activation related to spatial and nonspatial working memory, respectively. The delayed spatial alternation task increases LCGU rates bilaterally by 33-43% in the head of the caudate nucleus, where efferents from the dorsolateral prefrontal cortex project most densely. The delayed object alternation task enhances LCGU rates bilaterally by 32-37% in the body of the caudate nucleus, which is innervated by the temporal cortex. The visual pattern discrimination task similarly activated the body of the caudate, but in a smaller region and only in the right hemisphere. These findings provide the first evidence for metabolic activation of the caudate nuclei in working memory, supporting the role of this nucleus as a node in a neural network mediating DLPFC-dependent working memory processes. The double dissociation of activation observed suggests an anatomical and functional segregation of cortico-striatal circuits subserving spatial and nonspatial cognitive operations.
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Numerous studies have found selective involvement of the DMS in tasks requiring cognitive control and working memory.
“numerous studies have found selective involvement of the DMS in various tasks that require cognitive control and working memory [6,35,38]”
From Contributions of the striatum to learning, motivation, and performance: an associative account (2012) · cites this paper as [38]
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Cites
Parallel organization of functionally segregated circuits linking basal ganglia and cortex
Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.09.030186.002041 · Cited by 8,527 · see citing works
Sokoloff, L., Reivich, M., Kennedy, C., Rosiers, M. H. D., Patlak, C. S., Pettigrew, K. D., Sakurada, O., & Shinohara, M. (1977) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1977.tb10649.x · Cited by 6,000 · see citing works
Specific impairments of planning
Shallice, T. (1982) · Philosophical Transactions of the Royal Society of London. B, Biological Sciences · doi:10.1098/rstb.1982.0082 · Cited by 3,741 · see citing works
Higher cortical functions in man
Lurii︠a︡, A. R., Teuber, H., Pribram, K. H., & Haigh, B. (1966) · Basic Books · Cited by 2,858 · see citing works
Neuropathological Classification of Huntingtonʼs Disease
Vonsattel, J., Myers, R. H., STEVENS, T. J., Ferrante, R. J., Bird, E. D., & Richardson, E. P. (1985) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-198511000-00003 · Cited by 2,598 · see citing works
Fuster, J. M. (1997) · Cited by 2,095 · see citing works
Circuitry of Primate Prefrontal Cortex and Regulation of Behavior by Representational Memory
Goldman‐Rakic, P. S. (1987) · Comprehensive Physiology · doi:10.1002/cphy.cp010509 · Cited by 1,960 · see citing works
Self-citationSpatial working memory in humans as revealed by PET
Jonides, J. J., Smith, E. E., Koeppe, R. A., Awh, E., Minoshima, S., & Mintun, M. A. (1993) · Nature · doi:10.1038/363623a0 · Cited by 1,198 · see citing works
Chance Orders of Alternating Stimuli in Visual Discrimination Experiments
Gellermann, L. W. (1933) · The Pedagogical Seminary and Journal of Genetic Psychology · doi:10.1080/08856559.1933.10534237 · Cited by 1,187 · see citing works
The behavioural and motor consequences of focal lesions of the basal ganglia in man.
Bhatia, K., & Marsden, C. (1994) · Brain : a journal of neurology · doi:10.1093/brain/117.4.859 · Cited by 1,137 · see citing works
Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey
Selemon, L. D., & Goldman-Rakic, P. S. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-03-00776.1985 · Cited by 1,074 · see citing works
Self-citationDissociating Verbal and Spatial Working Memory Using PET
Smith, E. E., Jonides, J., & Koeppe, R. A. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.1.11 · Cited by 962 · see citing works
Cognitive deficits in Parkinson’s disease
Dubois, B., & Pillon, B. (1996) · Journal of Neurology · doi:10.1007/pl00007725 · Cited by 911 · see citing works
Object and Spatial Visual Working Memory Activate Separate Neural Systems in Human Cortex
Courtney, S. M., Ungerleider, L. G., Keil, K., & Haxby, J. V. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.1.39 · Cited by 891 · see citing works
FRONTAL LOBE DYSFUNCTION IN PARKINSON'S DISEASE
TAYLOR, A. E., Saint‐Cyr, J. A., & Lang, A. E. (1986) · Brain · doi:10.1093/brain/109.5.845 · Cited by 887 · see citing works
Neuronal correlate of pictorial short-term memory in the primate temporal cortexYasushi Miyashita
Miyashita, Y., & Chang, H. S. (1988) · Nature · doi:10.1038/331068a0 · Cited by 880 · see citing works
The `subcortical dementia' of progressive supranuclear palsy
Albert, M. L., Feldman, R. G., & Willis, A. L. (1974) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.37.2.121 · Cited by 871 · see citing works
FRONTO-STRIATAL COGNITIVE DEFICITS AT DIFFERENT STAGES OF PARKINSON'S DISEASE
Owen, A. M., James-Galton, M., Leigh, P. N., Summers, B. A., MARSDEN, C. D., Quinn, N. P., Lange, K. W., & Robbins, T. W. (1992) · Brain · doi:10.1093/brain/115.6.1727 · Cited by 859 · see citing works
Some effects of frontal lobectomy in man
Milner, B. A. (1964) · Medical Entomology and Zoology · Cited by 839 · see citing works
COGNITIVE DEFICITS IN THE EARLY STAGES OF PARKINSON'S DISEASE
Lees, A. J., & Smith, E. M. (1983) · Brain · doi:10.1093/brain/106.2.257 · Cited by 801 · see citing works
THE CORTICO-STRIATE PROJECTION IN THE MONKEY
Kemp, J. M., & Powell, T. P. S. (1970) · Brain · doi:10.1093/brain/93.3.525 · Cited by 798 · see citing works
Owen, A. M., Evans, A. C., & Petrides, M. (1996) · Cerebral Cortex · doi:10.1093/cercor/6.1.31 · Cited by 742 · see citing works
Activity of neurons in anterior inferior temporal cortex during a short- term memory task
Miller, E. K., Li, L., & Desimone, R. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-04-01460.1993 · Cited by 732 · see citing works
Petrides, M., Alivisatos, B., Evans, A. C., & Meyer, E. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.3.873 · Cited by 660 · see citing works
Yeterian, E. H., & Hoesen, G. W. V. (1978) · Brain Research · doi:10.1016/0006-8993(78)90059-8 · Cited by 641 · see citing works
Cooper, J. A., SAGAR, H. J., Jordan, N., Harvey, N. S., & Sullivan, E. V. (1991) · Brain · doi:10.1093/brain/114.5.2095 · Cited by 626 · see citing works
The orbital and medial prefrontal circuit through the primate basal ganglia
Haber, S., Kunishio, K., Mizobuchi, M., & Lynd-Balta, E. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-07-04851.1995 · Cited by 605 · see citing works
Hikosaka, O., Sakamoto, M., & Usui, S. (1989) · Journal of Neurophysiology · doi:10.1152/jn.1989.61.4.814 · Cited by 579 · see citing works
Behavioral effects of selective ablation of the caudate nucleus.
Divac, I., Rosvold, H. E., & Szwarcbart, M. K. (1967) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0024348 · Cited by 568 · see citing works
Spatial versus Object Working Memory: PET Investigations
Smith, E. E., Jonides, J. J., Koeppe, R. A., Awh, E., Schumacher, E. H., & Minoshima, S. (1995) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1995.7.3.337 · Cited by 512 · see citing works
An intricately patterned prefronto‐caudate projection in the rhesus monkey
Goldman, P. S., & Nauta, W. J. H. (1977) · The Journal of Comparative Neurology · doi:10.1002/cne.901710305 · Cited by 509 · see citing works
Mitchell, I., Clarke, C. E., Boyce, S., Robertson, R. G., Peggs, D., Sambrook, M. A., & Crossman, A. R. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90120-6 · Cited by 461 · see citing works
McCarthy, G., Blamire, A. M., Puce, A., Nobre, A. C., Bloch, G., Hyder, F., Goldman-Rakic, P., & Shulman, R. G. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.18.8690 · Cited by 459 · see citing works
Self-citationMetabolic Mapping of Functional Activity in the Hypothalamo-Neurohypophysial System of the Rat
Schwartz, W. J., Smith, C. B., Davidsen, L., Savaki, H., Sokoloff, L., Mata, M., Fink, D. J., & Gainer, H. (1979) · Science · doi:10.1126/science.462184 · Cited by 454 · see citing works
Planning and spatial working memory: A positron emission tomography study in humans
Owen, A. M., Doyon, J., Petrides, M., & Evans, A. C. (1996) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1996.tb01219.x · Cited by 450 · see citing works
Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey
Eblen, F., & Graybiel, A. M. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-09-05999.1995 · Cited by 391 · see citing works
Goldman, P. S., Rosvold, H. E., Vest, B., & Galkin, T. W. (1971) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0031649 · Cited by 381 · see citing works
Prefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys
Yeterian, E. H., & Pandya, D. N. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903120105 · Cited by 351 · see citing works
Saint‐Cyr, J. A., Ungerleider, L. G., & Desimone, R. (1990) · The Journal of Comparative Neurology · doi:10.1002/cne.902980202 · Cited by 319 · see citing works
Friedman, H., & Goldman-Rakic, P. S. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-02775.1994 · Cited by 311 · see citing works
Self-citationNeuronal activity in monkey striatum related to the expectation of predictable environmental events
Apicella, P., Scarnati, E., Ljungberg, T., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.68.3.945 · Cited by 305 · see citing works
Pillon, B., Dubois, B., Lhermitte, F., & Agid, Y. (1986) · Neurology · doi:10.1212/wnl.36.9.1179 · Cited by 291 · see citing works
Widespread corticostriate projections from temporal cortex of the rhesus monkey
Hoesen, G. W. V., Yeterian, E. H., & Lavizzo‐Mourey, R. J. (1981) · The Journal of Comparative Neurology · doi:10.1002/cne.901990205 · Cited by 264 · see citing works
Local cerebral glucose utilization in the normal conscious macaque monkey
Kennedy, C., Sakurada, O., Shinohara, M., Jehle, J. W., & Sokoloff, L. (1978) · Annals of Neurology · doi:10.1002/ana.410040402 · Cited by 245 · see citing works
Bättig, K., Rosvold, H. E., & Mishkin, M. (1960) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0047392 · Cited by 236 · see citing works
Gabrieli, J. D. E., Jaswinder, S., Stebbins, G. T., & Goetz, C. G. (1996) · Neuropsychology · doi:10.1037/0894-4105.10.3.321 · Cited by 211 · see citing works
Friedman, H., & Goldman-Rakic, P. S. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-12-04693.1988 · Cited by 210 · see citing works
Self-citationCorticostriatal connections of extrastriate visual areas in rhesus monkeys
Yeterian, E. H., & Pandya, D. Ν. (1995) · The Journal of Comparative Neurology · doi:10.1002/cne.903520309 · Cited by 202 · see citing works
Cavada, C., & Goldman-Rakic, P. S. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90037-o · Cited by 201 · see citing works
Self-citationSubcortical connections of inferior temporal areas TE and TEO in macaque monkeys
Webster, M. J., Bachevalier, J., & Ungerleider, L. G. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903350106 · Cited by 191 · see citing works
Neuronal activity in the monkey striatum during the initiation of movements
Schultz, W., & Romo, R. (1988) · Experimental Brain Research · doi:10.1007/bf00247503 · Cited by 171 · see citing works
Neurophysiology and cognitive functions of the striatum.
Rolls, E. T. (1995) · PubMed · Cited by 167 · see citing works
Visuospatial working memory in Parkinson's disease.
Bradley, V. A., Welch, J. L., & Dick, D. J. (1989) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.52.11.1228 · Cited by 151 · see citing works
Rosvold, H. E., Mishkin, M. M., & Szwarcbart, M. K. (1958) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0038337 · Cited by 127 · see citing works
Responses of striatal neurons in the behaving monkey. 2. Visual processing in the caudal neostriatum
Caan, W., Perrett, D. I., & Rolls, E. T. (1984) · Brain Research · doi:10.1016/0006-8993(84)90735-2 · Cited by 127 · see citing works
Partiot, A., Vérin, M., Pillon, B., Teixeira-Ferreira, C., Agid, Y., & Dubois, B. (1996) · Neuropsychologia · doi:10.1016/0028-3932(95)00143-3 · Cited by 117 · see citing works
Selective Delayed Response Deficits in Parkinson's and Alzheimer's Disease
Freedman, M., & Oscar‐Berman, M. (1986) · Archives of Neurology · doi:10.1001/archneur.1986.00520090026011 · Cited by 113 · see citing works
Oscar‐Berman, M., Zola-Morgan, S. M., Öberg, R. G. E., & Bonner, R. T. (1982) · Neuropsychologia · doi:10.1016/0028-3932(82)90009-4 · Cited by 93 · see citing works
Effect of caudate and septal nuclei lesions on resistance to extinction and delayed-alternation.
Butters, N., & Rosvold, H. E. (1968) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0025805 · Cited by 91 · see citing works
Effects of ventral putamen lesions on discrimination learning by monkeys.
Buerger, A. A., Gross, C. G., & Rocha‐Miranda, C. E. (1974) · Journal of Comparative and Physiological Psychology · doi:10.1037/h0036142 · Cited by 71 · see citing works
Subcortical connections of subdivisions of inferior temporal cortex in squirrel monkeys
Steele, G. E., & Weller, R. (1993) · Visual Neuroscience · doi:10.1017/s0952523800004776 · Cited by 52 · see citing works
Friedman, H. R., Janas, J. D., & Goldman‐Rakic, P. S. (1990) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.1990.2.1.18 · Cited by 52 · see citing works
Self-citationSm, C. (1972) · PubMed · Cited by 45 · see citing works
Yarowsky, P., Crane, A. M., & Sokoloff, L. (1985) · Brain Research · doi:10.1016/0006-8993(85)90226-4 · Cited by 14 · see citing works
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- Brandt J (1991) Cognitive impairments in Huntington's disease: insights into the neuropsychology of the striatum. In: Handbook of neuropsy- chology (Boller F, Grafman J, eds), pp 241-264. Amsterdam: Elsevier.
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Haber, S. N. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2003.10.003 · Cited by 1,479 · see citing works
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Olesen, P. J., Nagy, Z., Westerberg, H., & Klingberg, T. (2003) · Cognitive Brain Research · doi:10.1016/j.cogbrainres.2003.09.003 · Cited by 397 · see citing works
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Porrino, L. J., Lyons, D., Smith, H. R., Daunais, J. B., & Nader, M. A. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.5578-03.2004 · Cited by 276 · see citing works
Clatworthy, P. L., Lewis, S. J. G., Brichard, L., Hong, Y. T., Izquierdo, D., Clark, L., Cools, R., Aigbirhio, F. I., Baron, J.-C., Fryer, T. D., et al. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.3266-08.2009 · Cited by 229 · see citing works
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- Authors
- Levy, R., Friedman, H. R., Davachi, L., & Goldman-Rakic, P. S.
- Affiliations
- Yale University (US)
- ORCID
- Davachi, Lila
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1997-05-15
- Volume
- 17
- Issue
- 10
- Pages
- 3870-3882
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6573717
- OpenAlex
- W1600793774
- Cited by
- 279
- References
- 64
- Citations by year
- 2025: 3 · 2024: 6 · 2023: 5 · 2022: 5 · 2021: 7 · 2020: 4 · 2019: 7 · 2018: 3 · 2017: 8 · 2016: 11 · 2015: 7 · 2014: 8 · 2013: 12 · 2012: 11
- FWCI
- 6.80
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH 44866, MH38546, P50MH044866)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- caudate nucleus, working memory, spatial working memory, dorsolateral prefrontal cortex, striatum, local cerebral glucose utilization, visual pattern discrimination, sensorimotor tasks, corticostriatal circuits, temporal cortex, primate brain, metabolic activation
- MeSH terms
- Animals, Autoradiography, Caudate Nucleus, Conditioning, Psychological, Deoxyglucose, Macaca mulatta, Male, Memory, Pattern Recognition, Visual, Putamen, Spatial Behavior, Prefrontal Cortex
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