Mnemonic functions of the basal ganglia
Abstract
A synthesis of older and recent work on mnemonic functions of the basal ganglia in rats, monkeys and humans emphasizes a reciprocal relationship of the caudate nucleus and putamen with the cerebral cortex, which mediates the memory of consistent relationships between stimuli and responses (sometimes called habits) that often involve relationships between the individual and its environment (egocentric memory). Evidence at several levels of analysis (including neuroplastic synaptic changes, activity of single neurons, and behavioral changes caused by lesions or neurochemical manipulations) implicate dopamine release from nigro-striatal neurons in the reinforcement, or strengthening, of neural representations in the basal ganglia.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Stimulus-response or habit learning appears to be mediated, in part, by the dorsolateral striatum (or the putamen).
“This learning process appears to be mediated, in part, by the dorsolateral striatum (or the putamen) (Knowlton et al., 1996; White, 1997; Graybiel, 1998; Hikosaka, 1998; Yin and Knowlton, 2006).”
From Dopamine reward circuitry: Two projection systems from the ventral midbrain to the nucleus accumbens–olfactory tubercle complex (2007) · cites this paper as White, 1997
A circuit centered on dorsolateral striatum supports habit-based behavior.
“Related studies show that a circuit centered on dorsolateral striatum supports habit-based behavior (Yin et al., 2004, 2005; White, 1997; Balleine, 2005; Balleine and Dickinson, 1998; Killcross and Coutureau, 2003; Yin and Knowlton, 2006).”
From Goals and Habits in the Brain (2013) · cites this paper as White, 1997
Cites
Skinner, B. F., & Hull, C. L. (1944) · The American Journal of Psychology · doi:10.2307/1416955 · Cited by 4,061 · see citing works
Squire, L. R. (1984) · Springer eBooks · doi:10.1007/978-3-642-70094-1_32 · Cited by 2,126 · see citing works
A neostriatal habit learning system in humans
Knowlton, B. J., Mangels, J. A., & Squire, L. R. (1996) · Science · doi:10.1126/science.273.5280.1399 · Cited by 1,777 · see citing works
The amygdala: Neurobiological aspects of emotion, memory, and mental dysfunction.
Aggleton, J. P. (1992) · Wiley-Liss eBooks · Cited by 1,536 · see citing works
Packard, M. G., & McGaugh, J. L. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0007 · Cited by 1,505 · see citing works
Schultz, W., Apicella, P., & Ljungberg, T. (1993) · The Journal of Neuroscience · doi:10.1523/jneurosci.13-03-00900.1993 · Cited by 1,291 · see citing works
The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia
Gerfen, C. R. (1992) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.15.030192.001441 · Cited by 1,004 · see citing works
Motivational control of goal-directed action
Dickinson, A., & Balleine, B. (1994) · Animal Learning & Behavior · doi:10.3758/bf03199951 · Cited by 995 · see citing works
Responses of monkey dopamine neurons during learning of behavioral reactions
Ljungberg, T., Apicella, P., & Schultz, W. (1992) · Journal of Neurophysiology · doi:10.1152/jn.1992.67.1.145 · Cited by 987 · see citing works
Packard, M. G., Hirsh, R., & White, N. M. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01465.1989 · Cited by 971 · see citing works
Self-citationThe hippocampus and contextual retrieval of information from memory: A theory
Hirsh, R. (1974) · Behavioral Biology · doi:10.1016/s0091-6773(74)92231-7 · Cited by 957 · see citing works
A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum.
McDonald, R. J., & White, N. M. (1993) · Behavioral Neuroscience · doi:10.1037/0735-7044.107.1.3 · Cited by 885 · see citing works
Self-citationPreferential activation of midbrain dopamine neurons by appetitive rather than aversive stimuli
Mirenowicz, J., & Schultz, W. (1996) · Nature · doi:10.1038/379449a0 · Cited by 829 · see citing works
Long-term synaptic depression in the striatum: physiological and pharmacological characterization
Calabresi, P., Maj, R., Pisani, A., Mercuri, N. B., & Bernardi, G. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-11-04224.1992 · Cited by 673 · 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
Aosaki, T., Tsubokawa, H., Ishida, A., Watanabe, K., Graybiel, A. M., & Kimura, M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-06-03969.1994 · Cited by 600 · see citing works
Heindel, W. C., Salmon, D., Shults, C., Walicke, P. A., & Butters, N. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-02-00582.1989 · Cited by 582 · 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
Building action repertoires: memory and learning functions of the basal ganglia
Graybiel, A. M. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80100-6 · Cited by 557 · see citing works
Importance of unpredictability for reward responses in primate dopamine neurons
Mirenowicz, J., & Schultz, W. (1994) · Journal of Neurophysiology · doi:10.1152/jn.1994.72.2.1024 · Cited by 544 · see citing works
The corticostriatal projection: from synaptic plasticity to dysfunctions of the basal ganglia
Calabresi, P., Pisani, A., Mercuri, N. B., & Bernardi, G. (1996) · Trends in Neurosciences · doi:10.1016/0166-2236(96)81862-5 · Cited by 462 · see citing works
The Frontal Cortex-Basal Ganglia System in Primates
Wise, S. P., Murray, E. A., & Gerfen, C. R. (1996) · Critical Reviews in Neurobiology · doi:10.1615/critrevneurobiol.v10.i3-4.30 · Cited by 437 · see citing works
Aosaki, T., Graybiel, A. M., & Kimura, M. (1994) · Science · doi:10.1126/science.8023166 · Cited by 427 · see citing works
Calabresi, P., Pisani, A., Mercuri, N. B., & Bernardi, G. (1992) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1992.tb00119.x · Cited by 418 · see citing works
Packard, M. G., & White, N. M. (1991) · Behavioral Neuroscience · doi:10.1037//0735-7044.105.2.295 · Cited by 407 · see citing works
Self-citationHighly 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
Temporal and spatial characteristics of tonically active neurons of the primate's striatum
Aosaki, T., Kimura, M., & Graybiel, A. M. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.73.3.1234 · Cited by 385 · see citing works
Packard, M. G., & White, N. M. (1991) · Behavioral Neuroscience · doi:10.1037/0735-7044.105.2.295 · Cited by 334 · see citing works
Self-citationExperimentelle Beiträge zur Lehre vom Gedächtnis
Ephrussi, P. (1904) · University of Michigan Library Repository · Cited by 332 · see citing works
Input-output organization of the sensorimotor striatum in the squirrel monkey
Flaherty, A. W., & Graybiel, A. M. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00599.1994 · Cited by 329 · see citing works
Cortico-striate interrelations in the albino rat.
Webster, K. E. (1961) · PubMed · Cited by 328 · see citing works
Kesner, R., Bolland, B. L., & Dakis, M. (1993) · Experimental Brain Research · doi:10.1007/bf00229361 · Cited by 325 · see citing works
THE CORTICO-STRIATAL PROJECTION IN THE CAT.
Webster, K. E. (1965) · PubMed · Cited by 268 · see citing works
Caudate nucleus and memory for egocentric localization
Cook, D. G., & Kesner, R. P. (1988) · Behavioral and Neural Biology · doi:10.1016/s0163-1047(88)90338-x · Cited by 260 · see citing works
Activity in the caudate nucleus of monkey during spatial sequencing
Kermadi, I., & Joseph, J. (1995) · Journal of Neurophysiology · doi:10.1152/jn.1995.74.3.911 · Cited by 219 · see citing works
Neurobiology of skill and habit learning
Salmon, D. P., & Butters, N. (1995) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(95)80025-5 · Cited by 181 · see citing works
Neurophysiology and cognitive functions of the striatum.
Rolls, E. T. (1995) · PubMed · Cited by 167 · see citing works
A triple dissociation of memory systems: Hippocampus, amygdala, and dorsal striatum.
McDonald, R., & White, N. (1993) · Behavioral Neuroscience · doi:10.1037/a0034883 · Cited by 146 · see citing works
Self-citation“Cognitive” Functions of the Neostriatum
Öberg, R. G. E., & Divac, I. (1979) · Elsevier eBooks · doi:10.1016/b978-0-08-023174-7.50023-0 · Cited by 145 · see citing works
Retroactive impairment of passive avoidance learning by stimulation of the caudate nucleus
Wyers, E. J., Peeke, H. V. S., Williston, J. S., et al. (1968) · Experimental Neurology · doi:10.1016/0014-4886(68)90002-2 · Cited by 127 · see citing works
Basal ganglia — possible role in motor coordination and learning
HIKOSAKA, O. (1991) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(05)80042-x · Cited by 111 · see citing works
The caudate nucleus egocentric localization system.
Potegal, M. (1972) · PubMed · Cited by 109 · see citing works
White, N. M. (1989) · Life Sciences · doi:10.1016/0024-3205(89)90569-9 · Cited by 100 · see citing works
Self-citationGraybiel, A. M., Ohta, K., & Roffler-Tarlov, S. K. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-03-00720.1990 · Cited by 95 · see citing works
White, N. M., & Viaud, M. D. (1991) · Behavioral and Neural Biology · doi:10.1016/0163-1047(91)90609-t · Cited by 93 · see citing works
Self-citationNeuropsychological Differences Between the Dementias of Alzheimer's and Parkinson's Diseases
Huber, S. J., Shuttleworth, E. C., & Freidenberg, D. L. (1989) · Archives of Neurology · doi:10.1001/archneur.1989.00520480029015 · Cited by 89 · see citing works
Role of basal ganglia in behavioral learning
Kimura, M. (1995) · Neuroscience Research · doi:10.1016/0168-0102(95)00914-f · Cited by 82 · see citing works
Duration and nature of retrograde amnesia produced by stimulation of caudate nucleus
Wyers, E. J., & Deadwyler, S. A. (1971) · Physiology & Behavior · doi:10.1016/0031-9384(71)90075-8 · Cited by 81 · see citing works
Dissociation of visual and olfactory conditioning in the neostriatum of rats
Viaud, M. D., & White, N. M. (1989) · Behavioural Brain Research · doi:10.1016/s0166-4328(89)80069-5 · Cited by 76 · see citing works
Self-citationBehavior-related activity of primate dopamine neurons.
Schultz, W. (1995) · PubMed · Cited by 74 · see citing works
Lorenzini, C. A., Baldi, E., Bucherelli, C., et al. (1995) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1995.1008 · Cited by 66 · see citing works
Functions of the caudate nucleus.
Divac, I. (1968) · PubMed · Cited by 65 · see citing works
McGaugh, J. L., Introini-Collison, I. B., Juler, R. G., & Izquierdo, I. (1986) · Behavioral Neuroscience · doi:10.1037//0735-7044.100.6.839 · Cited by 63 · see citing works
Hippocampal function in the rat: Cognitive mapping or vicarious trial and error?
Amsel, A. (1993) · Hippocampus · doi:10.1002/hipo.450030302 · Cited by 55 · see citing works
White, N. M. (1988) · Life Sciences · doi:10.1016/0024-3205(88)90230-5 · Cited by 53 · see citing works
Self-citationIs cholinergic activity of the caudate nucleus involved in memory?
Prado-Alcalá, R. A. (1985) · Life Sciences · doi:10.1016/0024-3205(85)90563-6 · Cited by 53 · see citing works
McGaugh, J. L., Introini-Collison, I. B., Juler, R. G., et al. (1986) · Behavioral Neuroscience · doi:10.1037/0735-7044.100.6.839 · Cited by 50 · see citing works
Specificity of the memory deficits associated with basal ganglia dysfunction.
Butters, N., Salmon, D. P., & Heindel, W. C. (1995) · PubMed · Cited by 47 · see citing works
Effects of caudate and cortical lesions on place and response learning in rats
Thompson, W. G., Guilford, M. O., & HICKS, L. H. (1980) · Physiological Psychology · doi:10.3758/bf03326478 · Cited by 39 · see citing works
Packard, M. G., Introini-Collison, I. B., & McGaugh, J. L. (1996) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1996.0033 · Cited by 39 · see citing works
Time-dependent effects of cholinergic blockade of the striatum on memory
del Guante, M. Á. D., Cruz-Morales, S. E., & Prado-Alcalá, R. A. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90198-3 · Cited by 30 · see citing works
Caudate stimulation and retrograde amnesia: Amnesia threshold and gradient
Gold, P. E., & King, R. A. (1972) · Behavioral Biology · doi:10.1016/s0091-6773(72)80077-4 · Cited by 24 · see citing works
Motor Functions of the Striatum
Steg, G., & Johnels, B. (1979) · Elsevier eBooks · doi:10.1016/b978-0-08-023174-7.50020-5 · Cited by 19 · see citing works
Clinical validators: Comparisons of demented and amnesic patients.
Butters, N., Martone, M. E., White, B. E., et al. (1986) · American Psychological Association eBooks · doi:10.1037/10057-029 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Dissociable Roles of Ventral and Dorsal Striatum in Instrumental Conditioning
O'Doherty, J., Dayan, P., Schultz, J., Deichmann, R., Friston, K., & Dolan, R. J. (2004) · Science · doi:10.1126/science.1094285 · Cited by 2,088 · see citing works
Learning and Memory Functions of the Basal Ganglia
Packard, M. G., & Knowlton, B. J. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142937 · Cited by 1,717 · see citing works
Ikemoto, S. (2007) · Brain Research Reviews · doi:10.1016/j.brainresrev.2007.05.004 · Cited by 1,477 · see citing works
Ikemoto, S., & Panksepp, J. (1999) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00023-5 · Cited by 1,450 · see citing works
Dopamine and the regulation of cognition and attention
Nieoullon, A. (2002) · Progress in Neurobiology · doi:10.1016/s0301-0082(02)00011-4 · Cited by 1,131 · see citing works
The Basal Ganglia and Chunking of Action Repertoires
Graybiel, A. M. (1998) · Neurobiology of Learning and Memory · doi:10.1006/nlme.1998.3843 · Cited by 1,042 · see citing works
Nucleus accumbens shell and core dopamine: differential role in behavior and addiction
Di Chiara, G. (2002) · Behavioural Brain Research · doi:10.1016/s0166-4328(02)00286-3 · Cited by 996 · see citing works
Dolan, R. J., & Dayan, P. (2013) · Neuron · doi:10.1016/j.neuron.2013.09.007 · Cited by 977 · see citing works
depue, R. A., & morrone-strupinsky, J. V. (2005) · Behavioral and Brain Sciences · doi:10.1017/s0140525x05000063 · Cited by 958 · see citing works
Building neural representations of habits.
Jog, M. S., Kubota, Y., Connolly, C. I., Hillegaart, V., & Graybiel, A. M. (1999) · Science · doi:10.1126/science.286.5445.1745 · Cited by 834 · see citing works
Coordination of Actions and Habits in the Medial Prefrontal Cortex of Rats
Killcross, S. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.4.400 · Cited by 748 · see citing works
Perceptions of moral character modulate the neural systems of reward during the trust game
Delgado, M. R., Frank, R. H., & Phelps, E. A. (2005) · Nature Neuroscience · doi:10.1038/nn1575 · Cited by 729 · see citing works
Stress effects on memory: An update and integration
Schwabe, L., Joëls, M., Roozendaal, B., Wolf, O. T., & Oitzl, M. S. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.07.002 · Cited by 714 · see citing works
Actor–critic models of the basal ganglia: new anatomical and computational perspectives
Joel, D., Niv, Y., & Ruppin, E. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00047-3 · Cited by 500 · see citing works
Lesion to the nigrostriatal dopamine system disrupts stimulus-response habit formation
Faure, A., Haberland, U., Condé, F., & Massioui, N. E. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.3894-04.2005 · Cited by 402 · see citing works
Coutureau, E., & Killcross, S. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.025 · Cited by 342 · see citing works
Dopamine: a key regulator to adapt action, emotion, motivation and cognition
Nieoullon, A., & Coquerel, A. (2003) · Current Opinion in Neurology · doi:10.1097/00019052-200312002-00002 · Cited by 315 · see citing works
Pennartz, C. M. A., Lee, E., Verheul, J., Lipa, P., Barnes, C. A., & McNaughton, B. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0575-04.2004 · Cited by 282 · see citing works
Dissociating Hippocampal versus Basal Ganglia Contributions to Learning and Transfer
Myers, C. E., Shohamy, D., Gluck, M. A., Grossman, S., Kluger, A., Ferris, S., Golomb, J., Schnirman, G., & Schwartz, R. (2003) · Journal of Cognitive Neuroscience · doi:10.1162/089892903321208123 · Cited by 243 · see citing works
Neural Components Underlying Behavioral Flexibility in Human Reversal Learning
Ghahremani, D. G., Monterosso, J., Jentsch, J. D., Bilder, R. M., & Poldrack, R. A. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhp247 · Cited by 180 · see citing works
The human striatum is necessary for responding to changes in stimulus relevance.
Cools, R., Ivry, R. B., & D'Esposito, M. (2006) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2006.18.12.1973 · Cited by 122 · see citing works
- Authors
- White, N. M.
- Affiliations
- McGill University (CA)
- Corresponding author
- White, Norman M
- ORCID
- White, Norman M
- Venue
- Current Opinion in Neurobiology
- Publisher
- Elsevier BV
- Published
- 1997-04
- Volume
- 7
- Issue
- 2
- Pages
- 164-169
- ISSN
- 0959-4388 (ISSN-L)
- OpenAlex
- W1991503102
- Cited by
- 204
- References
- 65
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 4 · 2023: 1 · 2022: 4 · 2021: 2 · 2020: 3 · 2019: 2 · 2018: 5 · 2017: 6 · 2016: 2 · 2015: 1 · 2014: 6 · 2013: 3 · 2012: 2
- FWCI
- 1.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Current Opinion in Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Keywords
- basal ganglia, memory, caudate nucleus, putamen, nigrostriatal dopamine, habit formation, synaptic plasticity, single-unit activity, lesion studies, reinforcement, rats, monkeys, human
- MeSH terms
- Animals, Basal Ganglia, Memory, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review