Contributions of Striatal Subregions to Place and Response Learning

Yin, Henry H.; Knowlton, Barbara J.

doi:10.1101/lm.81004

Cited by 239Memory and Neural MechanismsSpatial Cognition and NavigationNeurotransmitter Receptor Influence on Behavior

Contributions of Striatal Subregions to Place and Response Learning

Open access

Yin, Henry H., Knowlton, Barbara J.·2004·Learning & Memory

DOI 10.1101/lm.81004PMC PMC498333

Open this paper in CoChat — free account Open PDF

Abstract

The involvement of different subregions of the striatum in place and response learning was examined using a T-maze. Rats were given NMDA lesions of the dorsolateral striatum (DLS), anterior dorsomedial striatum (ADMS), posterior dorsomedial striatum (PDMS), or sham surgery. They were then trained to retrieve food from the west arm of the maze, starting from the south arm, by turning left at the choice point. After 7 d of training, with four trials a day, a probe test was given in which the starting arm is inserted as the north arm, at the opposite side of the maze. A left turn would indicate a “response” strategy; a right turn, a “place” strategy. The rats were then trained for 7 more days, followed by a second probe test. Unlike rats in the other groups, most of the rats in the PDMS group turned left, using the response strategy on both probe tests. These results suggest that the PDMS plays a role in spatially guided behavior.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1101/lm.81004

Cites

28 of 28 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

The nucleus accumbens is strongly linked to behavioural flexibility and inhibitory control, including goal-directed and habitual behaviour.
“The nucleus accumbens is strongly linked to both behavioural flexibility and inhibitory control, including goal-directed and habitual behaviour [66–68].”
From Linking haploinsufficiency of the autism- and schizophrenia-associated gene Cyfip1 with striatal-limbic-cortical network dysfunction and cognitive inflexibility (2024) · cites this paper as [66]
The Discussion (page unavailable) links the posterior dorsomedial striatum to flexible, goal-directed responding, and the Abstract contrasts flexible place learning with stimulus-response habits. Our copy does not link these functions to the nucleus accumbens or address inhibitory control; searches for “nucleus accumbens” and “accumbens” found no relevant passage. (LLM, conf=0.86)
Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
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
Functional architecture of basal ganglia circuits: neural substrates of parallel processing
Alexander, G. E., & Crutcher, M. D. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90107-l · Cited by 4,131 · 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
Self-citation
Inactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning
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
The primate basal ganglia: Parallel and integrative networks
Haber, S. N. (2003) · Journal of Chemical Neuroanatomy · doi:10.1016/j.jchemneu.2003.10.003 · Cited by 1,479 · see citing works
The organization of the projection from the cerebral cortex to the striatum in the rat
McGeorge, A. J., & Faull, R. L. M. (1989) · Neuroscience · doi:10.1016/0306-4522(89)90128-0 · Cited by 1,345 · see citing works
Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems
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
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
Competition among multiple memory systems: converging evidence from animal and human brain studies
Poldrack, R. A., & Packard, M. G. (2003) · Neuropsychologia · doi:10.1016/s0028-3932(02)00157-4 · Cited by 880 · see citing works
Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat
Berendse, H. W., Graaf, Y. G.-D., & Groenewegen, H. J. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903160305 · Cited by 847 · see citing works
Cerebral hemisphere regulation of motivated behavior
Swanson, L. W. (2000) · Brain Research · doi:10.1016/s0006-8993(00)02905-x · Cited by 846 · see citing works
Extrinsic connections of the basal ganglia
Parent, A. (1990) · Trends in Neurosciences · doi:10.1016/0166-2236(90)90105-j · Cited by 633 · see citing works
Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: Further evidence for multiple memory systems.
Packard, M. G., & McGaugh, J. L. (1992) · Behavioral Neuroscience · doi:10.1037//0735-7044.106.3.439 · Cited by 555 · see citing works
The organization of the basal ganglia-thalamocortical circuits: Open interconnected rather than closed segregated
Joel, D., & Weiner, I. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90536-3 · Cited by 430 · see citing works
The role of prelimbic cortex in instrumental conditioning
Corbit, L. H., & Balleine, B. W. (2003) · Behavioural Brain Research · doi:10.1016/j.bbr.2003.09.023 · Cited by 423 · see citing works
Discrimination of cues in mazes: A resolution of the "place-vs.-response" question.
Restle, F. (1957) · Psychological Review · doi:10.1037/h0040678 · Cited by 386 · see citing works
Parallel Information Processing in the Dorsal Striatum: Relation to Hippocampal Function
Devan, B. D., & White, N. M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-07-02789.1999 · Cited by 366 · see citing works
Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning
Packard, M. G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.22.12881 · Cited by 290 · see citing works
Effects of medial and lateral caudate-putamen lesions on place- and cue-guided behaviors in the water maze: relation to thigmotaxis
Devan, B. D., McDonald, R. J., & White, N. M. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00107-7 · Cited by 288 · see citing works
Impairments in the acquisition, retention and selection of spatial navigation strategies after medial caudate-putamen lesions in rats
Whishaw, I. Q., Mittleman, G., Bunch, S., & Dunnett, S. B. (1987) · Behavioural Brain Research · doi:10.1016/0166-4328(87)90250-6 · Cited by 256 · 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
Acetylcholine actions in the dorsomedial striatum support the flexible shifting of response patterns
Ragozzino, M. E. (2003) · Neurobiology of Learning and Memory · doi:10.1016/s1074-7427(03)00077-7 · Cited by 93 · see citing works
The organization and collateralization of corticostriate neurones in the motor and sensory cortex of the rat brain
McGeorge, A. J., & Faull, R. L. M. (1987) · Brain Research · doi:10.1016/0006-8993(87)90855-9 · Cited by 92 · see citing works
Effects of US devaluation on win-stay and win-shift radial maze performance in rats.
Sage, J. R., & Knowlton, B. J. (2000) · Behavioral Neuroscience · doi:10.1037//0735-7044.114.2.295 · Cited by 90 · see citing works
Self-citation
Role of the Medial and Lateral Caudate-Putamen in Mediating an Auditory Conditional Response Association
Adams, S., Kesner, R. P., & Ragozzino, M. E. (2001) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2000.3989 · Cited by 57 · see citing works
Use of Win-Stay and Win-Shift Strategies in Place and Cue Tasks by Medial Caudate Putamen (MCPu) Lesioned Rats
Sakamoto, T., & Okaichi, H. (2001) · Neurobiology of Learning and Memory · doi:10.1006/nlme.2001.4006 · Cited by 23 · see citing works
Parallel Information Processing.
RASMUSSEN, E. M. (1992) · Cited by 16 · see citing works

Flagged first, then by citations

1 of the 29 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

Mishkin, M., Malamut, B., and Bachevalier, J. 1984. Memories and habits: Two neural systems. In Neurobiology of learning and memory (eds. G. Lynch et al.), pp. 65-77. Guilford Press, New York.

Sorted by citations

Autoradiographic localization of dopamine D1 and D2 receptors in rat nucleus accumbens: Resistance to differential rearing conditions
Bardo, M. T., & Hammer, R. P. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90226-e · Cited by 3,229 · see citing works
The role of the basal ganglia in habit formation
Yin, H. H., & Knowlton, B. J. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1919 · Cited by 2,402 · see citing works
Self-citation
Habits, Rituals, and the Evaluative Brain
Graybiel, A. M. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112851 · Cited by 1,697 · see citing works
The role of the dorsomedial striatum in instrumental conditioning
Yin, H. H., Ostlund, S. B., Knowlton, B. J., & Balleine, B. W. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04218.x · Cited by 1,099 · see citing works
Self-citation
Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits
Lerner, T. N., Shilyansky, C., Davidson, T. J., Evans, K. E., Beier, K. T., Zalocusky, K. A., Crow, A. K., Malenka, R. C., Luo, L., Tomer, R., et al. (2015) · Cell · doi:10.1016/j.cell.2015.07.014 · Cited by 794 · see citing works
“These regions of the dorsal striatum have been functionally distinguished by previous studies (Castañé et al., 2010; Faure et al., 2005; Featherstone and McDonald, 2004; Yin and Knowlton, 2004; Yin et al., 2004, 2005a, 2009, 2005b), leading us to hypothesize that SNc projections to these areas might also participate i…”
Method
Neural computations underlying arbitration between model-based and model-free learning
Lee, S. W., Shimojo, S., & O’Doherty, J. P. (2014) · Neuron · doi:10.1016/j.neuron.2013.11.028 · Cited by 642 · see citing works
Inactivation of dorsolateral striatum enhances sensitivity to changes in the action–outcome contingency in instrumental conditioning
YIN, H., KNOWLTON, B., & BALLEINE, B. (2006) · Behavioural Brain Research · doi:10.1016/j.bbr.2005.07.012 · Cited by 532 · see citing works
Self-citation
A unified framework for addiction: Vulnerabilities in the decision process
Redish, A. D., Jensen, S., & Johnson, A. (2008) · Behavioral and Brain Sciences · doi:10.1017/s0140525x0800472x · Cited by 501 · see citing works
Habitual alcohol seeking: time course and the contribution of subregions of the dorsal striatum
Corbit, L. H., Nie, H., & Janak, P. H. (2012) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.02.024 · Cited by 486 · see citing works
Reward-guided learning beyond dopamine in the nucleus accumbens: the integrative functions of cortico-basal ganglia networks
Yin, H. H., Ostlund, S. B., & Balleine, B. W. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06422.x · Cited by 416 · see citing works
Self-citation
Pavlovian to instrumental transfer: a neurobehavioural perspective.
Holmes, N. M., Marchand, A., & Coutureau, E. (2010) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.03.007 · Cited by 327 · see citing works
Altered mGluR5-Homer scaffolds and corticostriatal connectivity in a Shank3 complete knockout model of autism
Wang, X., Bey, A. L., Katz, B. M., Badea, A., Kim, N., David, L. K., Duffney, L. J., Kumar, S., Mague, S. D., Hulbert, S. W., et al. (2016) · Nature Communications · doi:10.1038/ncomms11459 · Cited by 318 · see citing works
Self-citation
Habits, action sequences and reinforcement learning
Dezfouli, A., & Balleine, B. W. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08050.x · Cited by 297 · see citing works
Integrating hippocampus and striatum in decision-making
Johnson, A. C., van der Meer, M. A. A., & Redish, A. D. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.01.003 · Cited by 254 · see citing works
Learning-related coordination of striatal and hippocampal theta rhythms during acquisition of a procedural maze task
DeCoteau, W. E., Thorn, C. A., Gibson, D. J., Courtemanche, R., Mitra, P. P., Kubota, Y., & Graybiel, A. M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700818104 · Cited by 239 · see citing works
Dorsal Striatal Circuits for Habits, Compulsions and Addictions
Lipton, D. M., Gonzales, B. J., & Citri, A. (2019) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2019.00028 · Cited by 197 · see citing works
Information Processing in Decision-Making Systems
van der Meer, M. A. A., Kurth-Nelson, Z. L., & Redish, A. D. (2012) · The Neuroscientist · doi:10.1177/1073858411435128 · Cited by 186 · see citing works
Primary food reward and reward‐predictive stimuli evoke different patterns of phasic dopamine signaling throughout the striatum
Brown, H. D., McCutcheon, J. E., Cone, J. J., Ragozzino, M. E., & Roitman, M. F. (2011) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2011.07914.x · Cited by 171 · see citing works
Neural Correlates of Forward Planning in a Spatial Decision Task in Humans
Simon, D. A., & Daw, N. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4647-10.2011 · Cited by 181 · see citing works
Striatal Contributions to Reward and Decision Making: Making Sense of Regional Variations in a Reiterated Processing Matrix
WICKENS, J. R., BUDD, C. S., HYLAND, B. I., & ARBUTHNOTT, G. W. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.016 · Cited by 165 · see citing works
Spatial goal coding in the hippocampal formation
Nyberg, N., Duvelle, É., Barry, C., & Spiers, H. J. (2022) · Neuron · doi:10.1016/j.neuron.2021.12.012 · Cited by 141 · see citing works
Maladaptive Bias for Extrahippocampal Navigation Strategies in Aging Humans
Wiener, J. M., de Condappa, O., Harris, M. A., & Wolbers, T. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0717-12.2013 · Cited by 161 · see citing works
Memory systems and the addicted brain
Goodman, J., & Packard, M. G. (2016) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2016.00024 · Cited by 140 · see citing works
Dissociation of memory systems: The story unfolds.
White, N. M., Packard, M. G., & McDonald, R. J. (2013) · Behavioral Neuroscience · doi:10.1037/a0034859 · Cited by 143 · see citing works
Some highlights of research on the effects of caudate nucleus lesions over the past 200 years
White, N. M. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.003 · Cited by 125 · see citing works
Plastic Corticostriatal Circuits for Action Learning
Costa, R. M. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.015 · Cited by 124 · see citing works
Integrating cortico-limbic-basal ganglia architectures for learning model-based and model-free navigation strategies
Khamassi, M., & Humphries, M. D. (2012) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2012.00079 · Cited by 121 · see citing works
The Sensorimotor Striatum Is Necessary for Serial Order Learning
Yin, H. H. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3989-10.2010 · Cited by 121 · see citing works
Self-citation
Neural correlates of stimulus-response and response-outcome associations in dorsolateral versus dorsomedial striatum
Stalnaker, T. A. (2010) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2010.00012 · Cited by 110 · see citing works
Ethanol reverses the direction of long‐term synaptic plasticity in the dorsomedial striatum
Yin, H. H., Park, B. S., Adermark, L., & Lovinger, D. M. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05606.x · Cited by 106 · see citing works
Self-citation
Striatal Versus Hippocampal Representations During Win-Stay Maze Performance
Berke, J. D., Breck, J. T., & Eichenbaum, H. (2009) · Journal of Neurophysiology · doi:10.1152/jn.91106.2008 · Cited by 105 · see citing works
Impaired Bidirectional Synaptic Plasticity and Procedural Memory Formation in Striatum-Specific cAMP Response Element-Binding Protein-Deficient Mice
Pittenger, C., Fasano, S., Mazzocchi‐Jones, D., Dunnett, S. B., Kandel, E. R., & Brambilla, R. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5406-05.2006 · Cited by 103 · see citing works
Loss of forebrain cholinergic neurons and impairment in spatial learning and memory in LHX7‐deficient mice
Fragkouli, A., Hearn, C. J., Errington, M. L., Cooke, S. F., Grigoriou, M. E., Bliss, T., Stylianopoulou, F., & Pachnis, V. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04141.x · Cited by 103 · see citing works
Rats Answer an Unexpected Question after Incidental Encoding
Zhou, W., Hohmann, A. G., & Crystal, J. D. (2012) · Current Biology · doi:10.1016/j.cub.2012.04.040 · Cited by 98 · see citing works
Exhumed from thought: Basal ganglia and response learning in the plus-maze
Packard, M. G. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.013 · Cited by 97 · see citing works
A theoretical account of cognitive effects in delay discounting
Kurth-Nelson, Z. L., Bickel, W. K., & Redish, A. D. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08058.x · Cited by 99 · see citing works
The Complex Nature of Hippocampal-Striatal Interactions in Spatial Navigation
Goodroe, S. C., Starnes, J., & Brown, T. I. (2018) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2018.00250 · Cited by 93 · see citing works
The Role of Dopamine in the Prelimbic Cortex and the Dorsomedial Striatum in Instrumental Conditioning
Lex, B., & Hauber, W. (2009) · Cerebral Cortex · doi:10.1093/cercor/bhp151 · Cited by 94 · see citing works
Hippocampal replay contributes to within session learning in a temporal difference reinforcement learning model
Johnson, A. C., & Redish, A. D. (2005) · Neural Networks · doi:10.1016/j.neunet.2005.08.009 · Cited by 91 · see citing works
Cooperative interactions between hippocampal and striatal systems support flexible navigation
Brown, T. I., Ross, R. S., Tobyne, S. M., & Stern, C. E. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2012.01.046 · Cited by 86 · see citing works
Representational changes of latent strategies in rat medial prefrontal cortex precede changes in behaviour
Powell, N. J., & Redish, A. D. (2016) · Nature Communications · doi:10.1038/ncomms12830 · Cited by 87 · see citing works
Homologous involvement of striatum and prefrontal cortex in rodent and human water maze learning
Woolley, D. G., Laeremans, A., Gantois, I., Mantini, D., Vermaercke, B., de Beeck, H. O., Swinnen, S. P., Wenderoth, N., Arckens, L., & D’Hooge, R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1217832110 · Cited by 84 · see citing works
Learning From Animal Models of Obsessive-Compulsive Disorder
Monteiro, P., & Feng, G. (2015) · Biological Psychiatry · doi:10.1016/j.biopsych.2015.04.020 · Cited by 79 · see citing works
Contributions of Medial Temporal Lobe and Striatal Memory Systems to Learning and Retrieving Overlapping Spatial Memories
Brown, T. I., & Stern, C. E. (2013) · Cerebral Cortex · doi:10.1093/cercor/bht041 · Cited by 76 · see citing works
Improving performance of robots using human-inspired approaches: a survey
Qiao, H., Zhong, S., Chen, Z., & Wang, H. (2022) · Science China Information Sciences · doi:10.1007/s11432-022-3606-1 · Cited by 76 · see citing works
Neural systems analysis of decision making during goal-directed navigation
Penner, M. R., & Mizumori, S. J. Y. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.08.010 · Cited by 72 · see citing works
Restriction of dopamine signaling to the dorsolateral striatum is sufficient for many cognitive behaviors
Darvas, M., & Palmiter, R. D. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907299106 · Cited by 75 · see citing works
The uncertainty processing theory of motivation
Anselme, P. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.020 · Cited by 75 · see citing works
Distinct sub-second dopamine signaling in dorsolateral striatum measured by a genetically-encoded fluorescent sensor
Salinas, A. G., Lee, J. O., Augustin, S. M., Zhang, S., Patriarchi, T., Tian, L., Morales, M., Mateo, Y., & Lovinger, D. M. (2023) · Nature Communications · doi:10.1038/s41467-023-41581-3 · Cited by 73 · see citing works
Anomalous neural circuit function in schizophrenia during a virtual Morris water task
Folley, B. S., Astur, R. S., Jagannathan, K., Calhoun, V. D., & Pearlson, G. D. (2009) · NeuroImage · doi:10.1016/j.neuroimage.2009.11.034 · Cited by 72 · see citing works
Contributions of Hippocampus and Striatum to Memory-Guided Behavior Depend on Past Experience
Ferbinteanu, J. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0840-16.2016 · Cited by 73 · see citing works
The influence of cannabinoids on learning and memory processes of the dorsal striatum
Goodman, J., & Packard, M. G. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.06.008 · Cited by 72 · see citing works
A general model of hippocampal and dorsal striatal learning and decision making
Geerts, J. P., Chersi, F., Stachenfeld, K., & Burgess, N. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2007981117 · Cited by 69 · see citing works
Reward Prediction Error Signaling in Posterior Dorsomedial Striatum Is Action Specific
Stalnaker, T. A., Calhoon, G. G., Ogawa, M., Roesch, M. R., & Schoenbaum, G. M. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0832-12.2012 · Cited by 65 · see citing works
A biologically inspired meta-control navigation system for the Psikharpax rat robot
Caluwaerts, K., Staffa, M., N’Guyen, S., Grand, C., Dollé, L., Favre-Félix, A., Girard, B., & Khamassi, M. (2012) · Bioinspiration & Biomimetics · doi:10.1088/1748-3182/7/2/025009 · Cited by 65 · see citing works
Memory systems 2018 – Towards a new paradigm
Ferbinteanu, J. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.11.005 · Cited by 66 · see citing works
Task complexity interacts with state-space uncertainty in the arbitration between model-based and model-free learning
Kim, D., Park, G. Y., O’Doherty, J. P., & Lee, S. W. (2019) · Nature Communications · doi:10.1038/s41467-019-13632-1 · Cited by 64 · see citing works
A study on the role of the dorsal striatum and the nucleus accumbens in allocentric and egocentric spatial memory consolidationPreprint
Leonibus, E. D., Oliverio, A., & Mele, A. (2005) · Learning & Memory · doi:10.1101/lm.94805 · Cited by 65 · see citing works
Habit Formation and the Striatum.
Knowlton, B., & Patterson, T. K. (2016) · Current topics in behavioral neurosciences · doi:10.1007/7854_2016_451 · Cited by 54 · see citing works
Self-citation
Different dorsal striatum circuits mediate action discrimination and action generalization
Hilário, M. R. F., Holloway, T. D., Jin, X., & Costa, R. M. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08073.x · Cited by 59 · see citing works
Multimodal Plasticity in Dorsal Striatum While Learning a Lateralized Navigation Task
Hawes, S., Evans, R. C., Unruh, B. A., Benkert, E. A., Gillani, F., Dumas, T. C., & Blackwell, K. T. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4415-14.2015 · Cited by 60 · see citing works
Voltage drives diverse endocannabinoid signals to mediate striatal microcircuit-specific plasticity
Mathur, B. N., Tanahira, C., Tamamaki, N., & Lovinger, D. M. (2013) · Nature Neuroscience · doi:10.1038/nn.3478 · Cited by 60 · see citing works
Computational validity: using computation to translate behaviours across species
Redish, A. D., Kepecs, Á., Anderson, L. M., Calvin, O. L., Grissom, N. M., Haynos, A. F., Heilbronner, S. R., Herman, A. B., Jacob, S., Ma, S., et al. (2021) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2020.0525 · Cited by 59 · see citing works
High on habits
Hilário, M. R. F. (2008) · Frontiers in Neuroscience · doi:10.3389/neuro.01.030.2008 · Cited by 59 · see citing works
The α2δ-1–NMDA receptor coupling is essential for corticostriatal long-term potentiation and is involved in learning and memory
Zhou, J., Li, D., Chen, S.-R., Luo, Y., & Pan, H. (2018) · Journal of Biological Chemistry · doi:10.1074/jbc.ra118.003977 · Cited by 56 · see citing works
Neural processing of reward in adolescent rodents
Simon, N. W., & Moghaddam, B. (2014) · Developmental Cognitive Neuroscience · doi:10.1016/j.dcn.2014.11.001 · Cited by 59 · see citing works
Path planning versus cue responding: a bio-inspired model of switching between navigation strategies
Dollé, L., Sheynikhovich, D., Girard, B., Chavarriaga, R., & Guillot, A. (2010) · Biological Cybernetics · doi:10.1007/s00422-010-0400-z · Cited by 58 · see citing works
Complementary Roles of the Hippocampus and the Dorsomedial Striatum during Spatial and Sequence-Based Navigation Behavior
Fouquet, C., Babayan, B. M., Watilliaux, A., Bontempi, B., Tobin, C., & Rondi‐Reig, L. (2013) · PLoS ONE · doi:10.1371/journal.pone.0067232 · Cited by 57 · see citing works
Contributions of dorsal striatal subregions to spatial alternation behaviorPreprint
Moussa, R., Poucet, B., Amalric, M., & Sargolini, F. (2011) · Learning & Memory · doi:10.1101/lm.2123811 · Cited by 56 · see citing works
Hippocampus and subregions of the dorsal striatum respond differently to a behavioral strategy change on a spatial navigation task
Regier, P. S., Amemiya, S., & Redish, A. D. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00189.2015 · Cited by 54 · see citing works
Motor, emotional and cognitive deficits in adult BACHD mice: A model for Huntington's disease
Abada, Y.-S. K., Schreiber, R., & Ellenbroek, B. A. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.10.039 · Cited by 53 · see citing works
Where is my reward and how do I get it? Interaction between the hippocampus and the basal ganglia during spatial learning
Retailleau, A., Etienne, S., Guthrie, M., & Boraud, T. (2011) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2011.10.002 · Cited by 52 · see citing works
Altered navigational strategy use and visuospatial deficits in hAPP transgenic mice
Deipolyi, A. R., Fang, S., Palop, J. J., Yu, G.-Q., Wang, X., & Mucke, L. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2006.10.021 · Cited by 52 · see citing works
A Computational Model of Craving and Obsession
Redish, A. D., & Johnson, A. C. (2007) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1390.014 · Cited by 49 · see citing works
Dopamine depletion in either the dorsomedial or dorsolateral striatum impairs egocentric Cincinnati water maze performance while sparing allocentric Morris water maze learning
Braun, A. A., Amos‐Kroohs, R. M., Gutierrez, A., Lundgren, K. H., Seroogy, K. B., Skelton, M. R., Vorhees, C. V., & Williams, M. T. (2014) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2014.10.009 · Cited by 51 · see citing works
Whole-Brain Mapping of Direct Inputs to Dopamine D1 and D2 Receptor-Expressing Medium Spiny Neurons in the Posterior Dorsomedial Striatum
Lu, J., Cheng, Y., Xie, X., Woodson, K., Bonifacio, J., Disney, E., Barbee, B. R., Wang, X., Zaidi, M., & Wang, J. (2020) · eNeuro · doi:10.1523/eneuro.0348-20.2020 · Cited by 51 · see citing works
Remembering the past and planning for the future in rats
Crystal, J. D. (2013) · Behavioural Processes · doi:10.1016/j.beproc.2012.11.014 · Cited by 50 · see citing works
Striatal and Medial Temporal Lobe Functional Interactions during Visuomotor Associative Learning
Mattfeld, A. T., & Stark, C. E. L. (2010) · Cerebral Cortex · doi:10.1093/cercor/bhq144 · Cited by 49 · see citing works
Interfacing behavioral and neural circuit models for habit formation
Lerner, T. N. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24581 · Cited by 46 · see citing works
The contribution of NMDA receptors in the dorsolateral striatum to egocentric response learning.
Palencia, C. A., & Ragozzino, M. E. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.4.953 · Cited by 49 · see citing works
Selective lesion of septal cholinergic neurons in rats impairs acquisition of a delayed matching to position T-maze task by delaying the shift from a response to a place strategy
Fitz, N. F., Gibbs, R. B., & Johnson, D. A. (2008) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2008.08.016 · Cited by 47 · see citing works
Virtual water maze learning in human increases functional connectivity between posterior hippocampus and dorsal caudate
Woolley, D. G., Mantini, D., Coxon, J. P., D’Hooge, R., Swinnen, S. P., & Wenderoth, N. (2014) · Human Brain Mapping · doi:10.1002/hbm.22700 · Cited by 45 · see citing works
Subregional specificity in human striatal habit learning: a meta-analytic review of the fMRI literature
Patterson, T. K., & Knowlton, B. J. (2017) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.10.005 · Cited by 47 · see citing works
Self-citation
Sensory representations in the striatum provide a temporal reference for learning and executing motor habits
Hidalgo-Balbuena, A. E., Luma, A. Y., Pimentel-Farfan, A. K., Peña-Rangel, T. M., & Rueda‐Orozco, P. E. (2019) · Nature Communications · doi:10.1038/s41467-019-12075-y · Cited by 47 · see citing works
Flexible use of allocentric and egocentric spatial memories activates differential neural networks in mice
Rinaldi, A., Leonibus, E. D., Cifra, A., Torromino, G., Minicocci, E., Sanctis, E. D., López‐Pedrajas, R., Oliverio, A., & Mele, A. (2020) · Scientific Reports · doi:10.1038/s41598-020-68025-y · Cited by 47 · see citing works
Striatum–hippocampus balance: From physiological behavior to interneuronal pathology
Ghiglieri, V., Sgobio, C., Costa, C., Picconi, B., & Calabresi, P. (2011) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2011.04.005 · Cited by 46 · see citing works
Place cell firing cannot support navigation without intact septal circuits
Bolding, K. A., Ferbinteanu, J., Fox, S. E., & Muller, R. U. (2019) · Hippocampus · doi:10.1002/hipo.23136 · Cited by 43 · see citing works
Place vs. Response Learning: History, Controversy, and Neurobiology
Goodman, J. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.598570 · Cited by 42 · see citing works
Changes in nucleus accumbens and neostriatal c‐Fos and DARPP‐32 immunoreactivity during different stages of food‐reinforced instrumental training
Segovia, K. N., Correa, M., Lennington, J. B., Conover, J. C., & Salamone, J. D. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08036.x · Cited by 40 · see citing works
Changes in brain oxidative metabolism induced by water maze training
Conejo, N. M., González‐Pardo, H., Vallejo, G., & Arias, J. L. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2006.11.057 · Cited by 42 · see citing works
The Michelin red guide of the brain: role of dopamine in goal-oriented navigation
Retailleau, A., & Boraud, T. (2014) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2014.00032 · Cited by 41 · see citing works
Subregion-specific modulation of excitatory input and dopaminergic output in the striatum by tonically activated glycine and GABAA receptors
Adermark, L. (2011) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2011.00085 · Cited by 41 · see citing works
Deliberation and Procedural Automation on a Two-Step Task for Rats
Hasz, B. M., & Redish, A. D. (2018) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2018.00030 · Cited by 41 · see citing works
Dichotomous parvalbumin interneuron populations in dorsolateral and dorsomedial striatum
Monteiro, P., Barak, B., Zhou, Y., McRae, R. E., Rodrigues, D., Wickersham, I. R., & Feng, G. (2018) · The Journal of Physiology · doi:10.1113/jp275936 · Cited by 41 · see citing works
The dorsomedial striatum mediates flexible choice behavior in spatial tasks
Braun, S., & Hauber, W. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.02.008 · Cited by 40 · see citing works
M 1 muscarinic activation induces long-lasting increase in intrinsic excitability of striatal projection neurons
Lv, X., Dickerson, J. W., Rook, J. M., Lindsley, C. W., Conn, P. J., & Xiang, Z. (2017) · Neuropharmacology · doi:10.1016/j.neuropharm.2017.03.017 · Cited by 40 · see citing works
Influence of Pre-Training Predator Stress on the Expression of c-fos mRNA in the Hippocampus, Amygdala, and Striatum Following Long-Term Spatial Memory Retrieval
VanElzakker, M., Zoladz, P., Thompson, V. M., Park, C. R., Halonen, J. D., Spencer, R. L., & Diamond, D. (2011) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2011.00030 · Cited by 41 · see citing works
Striatal activity in borderline personality disorder with comorbid intermittent explosive disorder: Sex differences
Pérez-Rodríguez, M. M., Hazlett, E. A., Rich, E. L., Ripoll, L. H., Weiner, D. M., Spence, N. Z., Goodman, M. S., Koenigsberg, H. W., Siever, L. J., & New, A. S. (2012) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2012.02.014 · Cited by 38 · see citing works
Applied neurophysiology of the horse; implications for training, husbandry and welfare
McBride, S. D., Parker, M. O., Roberts, K., & Hemmings, A. (2017) · Applied Animal Behaviour Science · doi:10.1016/j.applanim.2017.02.014 · Cited by 39 · see citing works
Emotion enhanced retention of cognitive skill learning.
Steidl, S., Razik, F., & Anderson, A. (2011) · Emotion · doi:10.1037/a0020288 · Cited by 42 · see citing works

The role of dopamine in the dorsomedial striatum in place and response learning
Lex, B., Sommer, S., & Hauber, W. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.10.081 · Cited by 24 · see citing works
Dorsolateral striatum implicated in the acquisition, but not expression, of immediate response learning in rodent submerged T-maze
Asem, J. S. A., & Holland, P. C. (2015) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2015.06.009 · Cited by 15 · see citing works
Re-thinking the role of the dorsal striatum in egocentric/response strategy
Botreau (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00007 · Cited by 9 · see citing works
Behavior strategy learning in rat: effects of lesions of the dorsal striatum or dorsal hippocampus
Compton, D. M. (2004) · Behavioural Processes · doi:10.1016/j.beproc.2004.06.002 · Cited by 64 · see citing works
Inability to acquire spatial information and deploy spatial search strategies in mice with lesions in dorsomedial striatum
Pooters, T., Gantois, I., Vermaercke, B., & D’Hooge, R. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.11.001 · Cited by 17 · see citing works

Authors: Yin, H. H., & Knowlton, B. J.
Affiliations: University of California, Los Angeles (US)
ORCID: Yin, Henry H.
Knowlton, Barbara J.
Venue: Learning & Memory
Publisher: Cold Spring Harbor Laboratory
Published: 2004-07
Volume: 11
Issue: 4
Pages: 459-463
ISSN: 1072-0502 (ISSN-L)
1549-5485
DOI: 10.1101/lm.81004
PMC: PMC498333
OpenAlex: W2121584908
Cited by: 238
References: 29
Citations by year: 2026: 6 · 2025: 3 · 2024: 13 · 2023: 10 · 2022: 7 · 2021: 13 · 2020: 12 · 2019: 13 · 2018: 11 · 2017: 8 · 2016: 15 · 2015: 13 · 2014: 12 · 2013: 12 · 2012: 19
Type: posted content
Language: en
Open access: bronze
doi.org
Locations: Learning & Memory (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Science Foundation (9985417)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Physical Sciences › Engineering › Automotive Engineering › Spatial Cognition and Navigation
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: striatum, dorsolateral striatum, dorsomedial striatum, place learning, response learning, spatial learning, NMDA lesions, T-maze, rats
MeSH terms: Animals, Brain Mapping, Choice Behavior, Male, Spatial Behavior, N-Methylaspartate, Neostriatum, Maze Learning, Rats, Long-Evans, 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

Contributions of Striatal Subregions to Place and Response Learning

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks