Structure and function of declarative and nondeclarative memory systems
Open accessAbstract
This article reviews recent studies of memory systems in humans and nonhuman primates. Three major conclusions from recent work are that (i) the capacity for nondeclarative (nonconscious) learning can now be studied in a broad array of tasks that assess classification learning, perceptuomotor skill learning, artificial grammar learning, and prototype abstraction; (ii) cortical areas adjacent to the hippocampal formation, including entorhinal, perirhinal, and parahippocampal cortices, are an essential part of the medial temporal lobe memory system that supports declarative (conscious) memory; and (iii) in humans, bilateral damage limited to the hippocampal formation is nevertheless sufficient to produce severe anterograde amnesia and temporally graded retrograde amnesia covering as much as 25 years.
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Neither the race model nor CMPL theory incorporates procedural knowledge in their learning mechanisms, because episodic memory is a type of declarative memory.
“Note that neither the race model nor the CMPL theory incorporates procedural knowledge (or memory) in their learning mechanisms, as episodic memory (storing instances) is a type of declarative memory (Squire & Zola, 1996).”
From Testing the three-stage model of second language skill acquisition (2025) · cites this paper as Squire & Zola, 1996
Declarative and nondeclarative memory systems are distinguished depending on the critical involvement of medial temporal lobe regions, particularly the hippocampus, in the acquisition of memory.
“In neuropsychology, declarative and nondeclarative memory systems are distinguished depending on the critical involvement of medial temporal lobe regions, particularly of the hippocampus, in the acquisition of memory (1134).”
From About Sleep's Role in Memory (2013) · cites this paper as [1134]
Nondeclarative memories can be acquired without involvement of medial temporal lobe structures.
“In contrast to declarative memories, nondeclarative memories can be acquired without involvement of medial temporal lobe structures (1134).”
From About Sleep's Role in Memory (2013) · cites this paper as [1134]
Cites
The Medial Temporal Lobe Memory System
Squire, L. R., & Zola-Morgan, S. (1991) · Science · doi:10.1126/science.1896849 · Cited by 3,282 · see citing works
Self-citationZola-Morgan, S., Squire, L., & Amaral, D. (1986) · The Journal of Neuroscience · doi:10.1523/jneurosci.06-10-02950.1986 · Cited by 1,997 · see citing works
Self-citationZola‐Morgan, S., Squire, L. R., & Ramus, S. J. (1994) · Hippocampus · doi:10.1002/hipo.450040410 · Cited by 362 · see citing works
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What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience?
Berridge, K. C., & Robinson, T. E. (1998) · Brain Research Reviews · doi:10.1016/s0165-0173(98)00019-8 · Cited by 4,127 · see citing works
Mesulam, M. (1998) · Brain · doi:10.1093/brain/121.6.1013 · Cited by 3,072 · see citing works
Rasch, B., & Born, J. (2013) · Physiological Reviews · doi:10.1152/physrev.00032.2012 · Cited by 2,783 · see citing works
Model of autism: increased ratio of excitation/inhibition in key neural systems
Rubenstein, J. L. R., & Merzenich, M. M. (2003) · Genes, Brain and Behavior · doi:10.1034/j.1601-183x.2003.00037.x · Cited by 2,768 · see citing works
Squire, L. R., Stark, C. E. L., & Clark, R. E. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144130 · Cited by 2,680 · see citing works
Self-citationBerridge, K. C., & Robinson, T. E. (2003) · Trends in Neurosciences · doi:10.1016/s0166-2236(03)00233-9 · Cited by 1,869 · 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
Chiesa, A., Calati, R., & Serretti, A. (2011) · Clinical Psychology Review · doi:10.1016/j.cpr.2010.11.003 · Cited by 1,295 · see citing works
Sleep-Dependent Learning and Memory Consolidation
Walker, M. P., & Stickgold, R. (2004) · Neuron · doi:10.1016/j.neuron.2004.08.031 · Cited by 1,113 · see citing works
Walker, M. P., & Stickgold, R. (2006) · Annual Review of Psychology · doi:10.1146/annurev.psych.56.091103.070307 · Cited by 1,075 · see citing works
The Anatomical Connections of the Macaque Monkey Orbitofrontal Cortex. A Review
Cavada, C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.3.220 · Cited by 917 · see citing works
Pike, K. E., Savage, G., Villemagne, V. L., Ng, S., Moss, S. A., Maruff, P., Mathis, C. A., Klunk, W. E., Masters, C. L., & Rowe, C. C. (2007) · Brain · doi:10.1093/brain/awm238 · Cited by 789 · see citing works
Topographical disorientation: a synthesis and taxonomy
Aguirre, G. K. (1999) · Brain · doi:10.1093/brain/122.9.1613 · Cited by 772 · 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
Pruessner, J. C. (2000) · Cerebral Cortex · doi:10.1093/cercor/10.4.433 · Cited by 706 · see citing works
Astill, R. G., Van der Heijden, K. B., Van IJzendoorn, M. H., & Van Someren, E. J. W. (2012) · Psychological Bulletin · doi:10.1037/a0028204 · Cited by 707 · see citing works
The whats and whens of sleep-dependent memory consolidation
Diekelmann, S., Wilhelm, I., & Born, J. (2009) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2008.08.002 · Cited by 566 · see citing works
Estrogen and cognitive functioning in women
Sherwin, B. B. (2003) · Endocrine Reviews · doi:10.1210/er.2001-0016 · Cited by 560 · see citing works
Early sleep triggers memory for early visual discrimination skills
Gais, S., Plihal, W., Wagner, U., & Born, J. (2000) · Nature Neuroscience · doi:10.1038/81881 · Cited by 558 · see citing works
Kim, J. J., Lee, H. J., Han, J.-S., & Packard, M. G. (2001) · The Journal of Neuroscience · doi:10.1523/jneurosci.21-14-05222.2001 · Cited by 537 · see citing works
The Declarative/Procedural Model of Lexicon and Grammar
Ullman, M. T. (2001) · Journal of Psycholinguistic Research · doi:10.1023/a:1005204207369 · Cited by 508 · see citing works
On the delay-dependent involvement of the hippocampus in object recognition memory
HAMMOND, R. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.03.005 · Cited by 476 · see citing works
Endophenotypes in the Genetic Analyses of Mental Disorders
Cannon, T. D., & Keller, M. C. (2006) · Annual Review of Clinical Psychology · doi:10.1146/annurev.clinpsy.2.022305.095232 · Cited by 399 · see citing works
Ranganath, C. (2010) · Hippocampus · doi:10.1002/hipo.20852 · Cited by 375 · see citing works
Cognitive functions of the basal forebrain
Baxter, M. G., & Chiba, A. A. (1999) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(99)80024-5 · Cited by 351 · see citing works
Neural bases of food-seeking: affect, arousal and reward in corticostriatolimbic circuits
BALLEINE, B. (2005) · Physiology & Behavior · doi:10.1016/j.physbeh.2005.08.061 · Cited by 326 · see citing works
Modulation of memory by insulin and glucose: Neuropsychological observations in Alzheimer’s disease
Watson, G. S., & Craft, S. (2004) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2004.02.048 · Cited by 307 · see citing works
Hippocampal involvement in contextual modulation of fear extinction
Ji, J., & Maren, S. (2007) · Hippocampus · doi:10.1002/hipo.20331 · Cited by 297 · see citing works
Intranasal Insulin Improves Memory in Humans: Superiority of Insulin Aspart
Benedict, C., Hallschmid, M., Schmitz, K., Schultes, B., Ratter, F., Fehm, H. L., Born, J., & Kern, W. (2007) · Neuropsychopharmacology · doi:10.1038/sj.npp.1301193 · Cited by 302 · see citing works
Moita, M. A. P., Rosis, S., Zhou, Y., LeDoux, J. E., & Blair, H. T. (2003) · Neuron · doi:10.1016/s0896-6273(03)00033-3 · Cited by 295 · see citing works
Benedict, C., Kern, W., Schultes, B., Born, J., & Hallschmid, M. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2606 · Cited by 296 · see citing works
Sleep and memory in healthy children and adolescents - a critical review
Kopasz, M., Loessl, B., Hornyak, M., Riemann, D., Nissen, C., Piosczyk, H., & Voderholzer, U. (2010) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2009.10.006 · Cited by 277 · see citing works
Association of childhood trauma with cognitive function in healthy adults: a pilot study
Majer, M., Nater, U. M., Lin, J.-M. S., Capuron, L., & Reeves, W. C. (2010) · BMC Neurology · doi:10.1186/1471-2377-10-61 · Cited by 281 · see citing works
Reinforcement learning in depression: a review of computational research
Chen, C., Takahashi, T., Nakagawa, S., Inoue, T., & Kusumi, I. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2015.05.005 · Cited by 233 · see citing works
The human perirhinal cortex and semantic memory
Davies, R. R., Graham, K. S., Xuereb, J. H., Williams, G. B., & Hodges, J. R. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03710.x · Cited by 238 · see citing works
Episodic memory: what can animals remember about their past?
Griffiths, D., Dickinson, A., & Clayton, N. (1999) · Trends in Cognitive Sciences · doi:10.1016/s1364-6613(98)01272-8 · Cited by 228 · see citing works
Habitual use of GPS negatively impacts spatial memory during self-guided navigation
Dahmani, L., & Bohbot, V. D. (2020) · Scientific Reports · doi:10.1038/s41598-020-62877-0 · Cited by 212 · see citing works
Out-of-body-induced hippocampal amnesia
Bergouignan, L., Nyberg, L., & Ehrsson, H. H. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1318801111 · Cited by 199 · see citing works
Kaplan, R. J., Greenwood, C. E., Winocur, G., & Wolever, T. M. (2000) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/72.3.825 · Cited by 193 · see citing works
Use it or lose it: how neurogenesis keeps the brain fit for learning
Shors, T. J., Anderson, M. L., Curlik, D. M., & Nokia, M. S. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.04.023 · Cited by 190 · see citing works
Role of the Basal Ganglia in Category Learning: How Do Patients With Parkinson's Disease Learn?
Shohamy, D., Myers, C. E., Onlaor, S., & Gluck, M. A. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.4.676 · Cited by 186 · see citing works
Kim, J. J., Koo, J. W., Lee, H. J., & Han, J.-S. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4623-04.2005 · Cited by 184 · see citing works
Sleep and memory in mammals, birds and invertebrates
Vorster, A. P., & Born, J. (2015) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.09.020 · Cited by 169 · see citing works
A quantitative morphometric comparative analysis of the primate temporal lobe
Rilling, J. K., & Seligman, R. A. (2002) · Journal of Human Evolution · doi:10.1006/jhev.2001.0537 · Cited by 172 · see citing works
Obese men respond to cognitive but not to catabolic brain insulin signaling
Hallschmid, M., Benedict, C., Schultes, B., Born, J., & Kern, W. (2008) · International Journal of Obesity · doi:10.1038/sj.ijo.0803722 · Cited by 165 · see citing works
Sleep-dependent memory consolidation – What can be learnt from children?
Wilhelm, I., Prehn-Kristensen, A., & Born, J. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2012.03.002 · Cited by 161 · see citing works
A distributed representation of internal time
Howard, M. W., Shankar, K. H., Aue, W. R., & Criss, A. H. (2015) · Psychological Review · doi:10.1037/a0037840 · Cited by 133 · see citing works
The social neuroscience of intergroup relations
Amodio, D. M. (2008) · European Review of Social Psychology · doi:10.1080/10463280801927937 · Cited by 118 · see citing works
Cooperation between the hippocampus and the striatum during episodic encoding
Sadeh, T., Shohamy, D., Levy, D. R., Reggev, N., & Maril, A. (2011) · Journal of Cognitive Neuroscience · doi:10.1162/jocn.2010.21549 · Cited by 104 · see citing works
Giménez, M., Junqué, C., Narberhaus, A., Caldú, X., Salgado-Pineda, P., Bargalló, N., Segarra, D., & Botet, F. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.07.029 · Cited by 94 · see citing works
Age-related differences in sleep-based memory consolidation: a meta-analysis
Gui, W.-J., Li, H.-J., Guo, Y.-H., Peng, P., Lei, X., & Yu, J. (2017) · Neuropsychologia · doi:10.1016/j.neuropsychologia.2017.02.001 · Cited by 78 · see citing works
Cortical–hippocampal coupling during manifold exploration in motor cortex
Kim, J., Joshi, A., Frank, L., & Ganguly, K. (2023) · Nature · doi:10.1038/s41586-022-05533-z · Cited by 77 · see citing works
Grillon, C. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.04.017 · Cited by 80 · see citing works
“Explicit learning requires an intact temporal lobe (hippocampus and related cortical areas), but implicit learning can be demonstrated in patients with hippocampal damage (34).”
Cognitive neuroscience perspective on memory: overview and summary
Sridhar, S., Khamaj, A., & Asthana, M. K. (2023) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2023.1217093 · Cited by 80 · see citing works
Barbosa, F. F., Santos, J. R., Meurer, Y. S. R., Macêdo, P. T., Ferreira, L. M. S., Pontes, I. M. O., Ribeiro, A. M., & Silva, R. H. (2013) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2013.00112 · Cited by 79 · see citing works
“Although hippocampal function is essential to human episodic memory (Squire and Zola, 1996; Tulving, 2002), the results regarding the role of this structure in the OR in rodents are controversial (Brown and Aggleton, 2001; Aggleton and Brown, 2006; Ainge et al., 2006).”
BackgroundYoshida, T., McCarley, R. W., Nakamura, M., Lee, K., Koo, M.-S., Bouix, S., Salisbury, D. F., Morra, L., Shenton, M. E., & Niznikiewicz, M. A. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.05.004 · Cited by 74 · see citing works
West, G. L., Drisdelle, B. L., Konishi, K., Jackson, J., Jolicoeur, P., & Bohbot, V. D. (2015) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2014.2952 · Cited by 70 · see citing works
Sleep-dependent memory processing
Walker, M. P. (2008) · Harvard Review of Psychiatry · doi:10.1080/10673220802432517 · Cited by 72 · see citing works
Sleep-dependent motor memory consolidation in healthy adults: a meta-analysis
Schmid, D., Erlacher, D., Klostermann, A., Kredel, R., & Hossner, E.-J. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.07.028 · Cited by 58 · see citing works
Emotion, higher-order syntactic thoughts, and consciousness
Rolls, E. T. (2008) · Frontiers of ConsciousnessChichele Lectures · doi:10.1093/acprof:oso/9780199233151.003.0004 · Cited by 51 · see citing works
Transitive inference in adults with autism spectrum disorders
Solomon, M., Frank, M. J., Smith, A. C., Ly, S., & Carter, C. S. (2011) · Cognitive, Affective, & Behavioral Neuroscience · doi:10.3758/s13415-011-0040-3 · Cited by 29 · see citing works
Manns, J. R., & Eichenbaum, H. (2007) · Evolution of Nervous Systems · doi:10.1016/b0-12-370878-8/00086-0 · Cited by 28 · see citing works
Parallel explicit and implicit control of reaching
Mazzoni, P., & Wexler, N. S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007557 · Cited by 24 · see citing works
Gendron, M., Mesquita, B., & Barrett, L. F. (2020) · Culture, Mind, and Brain · doi:10.1017/9781108695374.010 · Cited by 20 · see citing works
Brünner, Y. F., Rodriguez-Raecke, R., Mutic, S., Benedict, C., & Freiherr, J. (2016) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2016.07.027 · Cited by 17 · see citing works
Implicit and explicit reward learning in chronic nicotine use
Paelecke-Habermann, Y., Paelecke, M., Giegerich, K., Reschke, K., & Kübler, A. (2013) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2012.09.004 · Cited by 13 · see citing works
Silagi, M. L., Ferreira, O. P., Almeida, I. J. D., Simões, J. D. S., Zampieri, S. A., Santana, B. R. F. D., & Mansur, L. L. (2020) · Dementia & Neuropsychologia · doi:10.1590/1980-57642020dn14-020002 · Cited by 9 · see citing works
Testing the three-stage model of second language skill acquisition
Maie, R., & Godfroid, A. (2025) · Studies in Second Language Acquisition · doi:10.1017/s027226312500021x · Cited by 5 · see citing works
“Note that neither the race model nor the CMPL theory incorporates procedural knowledge (or memory) in their learning mechanisms, as episodic memory (storing instances) is a type of declarative memory (Squire & Zola, 1996).”
Silva Sánchez, M., Lainez Quinde, G. A., & Zambrano Vélez, W. A. (2026) · Education Sciences · doi:10.3390/educsci16060962
“According to Squire and Zola (1996), this system is involuntary and consists of procedural memory for motor skills and habits, associative and non-associative learning driven by environmental conditioning, and priming, which improves information recognition based on previous exposure.”
- Authors
- Squire, L. R., & Zola, S. M.
- Affiliations
- University of California San Diego (US)
- Veterans Health Administration (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1996-11-26
- Volume
- 93
- Issue
- 24
- Pages
- 13515-13522
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC33639
- OpenAlex
- W2019044369
- Cited by
- 1,327
- References
- 3
- Citations by year
- 2026: 19 · 2025: 32 · 2024: 40 · 2023: 40 · 2022: 40 · 2021: 40 · 2020: 75 · 2019: 53 · 2018: 52 · 2017: 54 · 2016: 40 · 2015: 46 · 2014: 57 · 2013: 80 · 2012: 66
- FWCI
- 2.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01ns019063-12)
- National Institute of Mental Health (R37MH024600, R01MH024600, MH24600)
- National Institute of Neurological Disorders and Stroke (NS19063)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Cognitive Functions and Memory
- Keywords
- declarative memory, implicit memory, classification learning, artificial grammar learning, hippocampal formation, entorhinal cortex, perirhinal cortex, parahippocampal cortex, medial temporal lobe, anterograde amnesia, retrograde amnesia, non-human primates
- MeSH terms
- Amnesia, Amnesia, Retrograde, Animals, Haplorhini, Brain, Hippocampus, Humans, Learning, Memory, Models, Neurological, Models, Psychological, Primates, Temporal Lobe
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