Conscious and Unconscious Memory Systems the Discovery of Declarative and Nondeclarative Memory Systems

The idea that memory is not a single mental faculty has a long and interesting history but became a topic of experimental and biologic inquiry only in the mid-20th century. It is now clear that there are different kinds of memory, which are supported by different brain systems. One major distinction can be drawn between working memory and long-term memory. Long-term memory can be separated into declarative (explicit) memory and a collection of nondeclarative (implicit) forms of memory that include habits, skills, priming, and simple forms of conditioning. These memory systems depend variously on the hippocampus and related structures in the parahippocampal gyrus, as well as on the amygdala, the striatum, cerebellum, and the neocortex. This work recounts the discovery of declarative and nondeclarative memory and then describes the nature of declarative memory, working memory, nondeclarative memory, and the relationship between memory systems.

[1]  A. Graybiel Habits, rituals, and the evaluative brain. , 2008, Annual review of neuroscience.

[2]  David C Rowland,et al.  Place cells, grid cells, and memory. , 2015, Cold Spring Harbor perspectives in biology.

[3]  C. Gilbert,et al.  Adult Visual Cortical Plasticity , 2012, Neuron.

[4]  Jonathan R. Whitlock,et al.  Navigating from hippocampus to parietal cortex , 2008, Proceedings of the National Academy of Sciences.

[5]  L. Squire,et al.  Parallel brain systems for learning with and without awareness. , 1994, Learning & memory.

[6]  L. Squire,et al.  Robust habit learning in the absence of awareness and independent of the medial temporal lobe , 2005, Nature.

[7]  R. J. McDonald,et al.  How does a specific learning and memory system in the mammalian brain gain control of behavior? , 2013, Hippocampus.

[8]  Jelliffe,et al.  Matter and Memory , 1896 .

[9]  Ralph Adolphs,et al.  The Biology of Fear , 2013, Current Biology.

[10]  L R Squire,et al.  Intact perceptual memory in the absence of conscious memory. , 1997, Behavioral neuroscience.

[11]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[12]  E. Vogel,et al.  Discrete capacity limits in visual working memory , 2010, Current Opinion in Neurobiology.

[13]  M. Gluck,et al.  Interactive memory systems in the human brain , 2001, Nature.

[14]  A. Dickinson,et al.  Episodic-like memory during cache recovery by scrub jays , 1998, Nature.

[15]  Richard C. Atkinson,et al.  Human Memory: A Proposed System and its Control Processes , 1968, Psychology of Learning and Motivation.

[16]  M. Packard,et al.  Factors that influence the relative use of multiple memory systems , 2013, Hippocampus.

[17]  L. Squire,et al.  Perceptual learning, awareness, and the hippocampus , 2001, Hippocampus.

[18]  D. Gaffan,et al.  Recognition impaired and association intact in the memory of monkeys after transection of the fornix. , 1974, Journal of comparative and physiological psychology.

[19]  John M Hoffman,et al.  Ecstasy and Agony: Activation of the Human Amygdala in Positive and Negative Emotion , 2002, Psychological science.

[20]  Joseph E LeDoux,et al.  Active Avoidance Learning Requires Prefrontal Suppression of Amygdala-Mediated Defensive Reactions , 2013, The Journal of Neuroscience.

[21]  Hauke Bartsch,et al.  Postmortem examination of patient H.M.’s brain based on histological sectioning and digital 3D reconstruction , 2014, Nature Communications.

[22]  C. Semenza,et al.  A selective deficit in the production of exact musical intervals following right‐hemisphere damage , 2004, Cognitive neuropsychology.

[23]  W. Schultz Updating dopamine reward signals , 2013, Current Opinion in Neurobiology.

[24]  A. Baddeley,et al.  Amnesia and the distinction between long- and short-term memory. , 1970 .

[25]  B. Milner,et al.  Disorders of learning and memory after temporal lobe lesions in man. , 1972, Clinical neurosurgery.

[26]  J. D. McGaugh,et al.  Inactivation of Hippocampus or Caudate Nucleus with Lidocaine Differentially Affects Expression of Place and Response Learning , 1996, Neurobiology of Learning and Memory.

[27]  H. Eichenbaum,et al.  Conservation of hippocampal memory function in rats and humans , 1996, Nature.

[28]  Alex Martin,et al.  Properties and mechanisms of perceptual priming , 1998, Current Opinion in Neurobiology.

[29]  M. Chun,et al.  Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage , 1999, Nature Neuroscience.

[30]  Kyle S. Smith,et al.  A dual operator view of habitual behavior reflecting cortical and striatal dynamics. , 2013, Neuron.

[31]  Larry R Squire,et al.  Intact Working Memory for Relational Information after Medial Temporal Lobe Damage , 2010, The Journal of Neuroscience.

[32]  C. Büchel,et al.  The Role of Medial Temporal Lobe Structures in Implicit Learning An Event-Related fMRI Study , 2002, Neuron.

[33]  G. Quirk,et al.  Fear extinction as a model for translational neuroscience: ten years of progress. , 2012, Annual review of psychology.

[34]  M. Leyton,et al.  Caudate nucleus-dependent navigational strategies are associated with increased use of addictive drugs , 2013, Hippocampus.

[35]  L. Davachi Item, context and relational episodic encoding in humans , 2006, Current Opinion in Neurobiology.

[36]  E. Tolman Cognitive maps in rats and men. , 1948, Psychological review.

[37]  E. Tulving Elements of episodic memory , 1983 .

[38]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[39]  C. Stern,et al.  An fMRI Study of the Role of the Medial Temporal Lobe in Implicit and Explicit Sequence Learning , 2003, Neuron.

[40]  P. Goldman-Rakic Architecture of the Prefrontal Cortex and the Central Executive , 1995, Annals of the New York Academy of Sciences.

[41]  E. Kandel,et al.  The Molecular and Systems Biology of Memory , 2014, Cell.

[42]  The Wernicke–Korsakoff Syndrome and Related Neurological Disorders Due to Alcoholism and Malnutrition (2nd edn). M. Victor, R. D. Adams and G. Collins. Philadelphia: F. A. Davis Co. 1989. 231 pp. $55.00. , 1990 .

[43]  C. Gilbert,et al.  Perceptual learning and adult cortical plasticity , 2009, The Journal of physiology.

[44]  Faraneh Vargha-Khadem,et al.  Is the hippocampus necessary for visual and verbal binding in working memory? , 2010, Neuropsychologia.

[45]  L. Squire,et al.  Memory: brain systems and behavior , 1988, Trends in Neurosciences.

[46]  J. D. McGaugh,et al.  Drug enhancement of memory consolidation: historical perspective and neurobiological implications , 2008, Psychopharmacology.

[47]  Andy C. H. Lee,et al.  Going beyond LTM in the MTL: A synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception , 2010, Neuropsychologia.

[48]  Endel Tulving,et al.  Remembering and Knowing the Past , 2016 .

[49]  Michael Davis,et al.  Neural systems involved in fear and anxiety measured with fear-potentiated startle. , 2006, The American psychologist.

[50]  Alan Baddeley,et al.  Double Dissociations: Not Magic, but Still Useful , 2003, Cortex.

[51]  J. Kril,et al.  Degeneration of anterior thalamic nuclei differentiates alcoholics with amnesia. , 2000, Brain : a journal of neurology.

[52]  G. Ryle,et al.  心的概念 = The concept of mind , 1962 .

[53]  Y. Miyashita,et al.  Formation of mnemonic neuronal responses to visual paired associates in inferotemporal cortex is impaired by perirhinal and entorhinal lesions. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[54]  N. Turk-Browne,et al.  Mechanisms for widespread hippocampal involvement in cognition. , 2013, Journal of experimental psychology. General.

[55]  Jennifer A. Mangels,et al.  A Neostriatal Habit Learning System in Humans , 1996, Science.

[56]  D. Schacter,et al.  Priming and the Brain , 1998, Neuron.

[57]  G Mandler,et al.  The information that amnesic patients do not forget. , 1984, Journal of experimental psychology. Learning, memory, and cognition.

[58]  Nicholas B. Turk-Browne,et al.  Memory-guided attention: control from multiple memory systems , 2012, Trends in Cognitive Sciences.

[59]  Guillén Fernández,et al.  The right hippocampus participates in short-term memory maintenance of object–location associations , 2006, NeuroImage.

[60]  S. Corkin,et al.  H.M.'s contributions to neuroscience: A review and autopsy studies , 2014, Hippocampus.

[61]  N. Cowan The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[62]  Adam Gazzaley,et al.  Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load. , 2008, Cerebral cortex.

[63]  L. Squire,et al.  Intact Conceptual Priming in the Absence of Declarative Memory , 2004, Psychological science.

[64]  L R Squire,et al.  On the contribution of perceptual fluency and priming to recognition memory , 2005, Cognitive, affective & behavioral neuroscience.

[65]  H. Eichenbaum,et al.  Critical role of the hippocampus in memory for sequences of events , 2002, Nature Neuroscience.

[66]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[67]  R. Poldrack,et al.  Competition among multiple memory systems: converging evidence from animal and human brain studies , 2003, Neuropsychologia.

[68]  Larry R Squire,et al.  Declarative Memory, Awareness, and Transitive Inference , 2005, The Journal of Neuroscience.

[69]  R. F. Thompson,et al.  Organization of memory traces in the mammalian brain. , 1994, Annual review of neuroscience.

[70]  J. Deese Principles of Psychology , 1923, Nature.

[71]  M. Mishkin Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus , 1978, Nature.

[72]  H. Markowitsch Diencephalic amnesia: a reorientation towards tracts? , 1988, Brain Research Reviews.

[73]  Lars Schwabe,et al.  Stress and the engagement of multiple memory systems: Integration of animal and human studies , 2013, Hippocampus.

[74]  Robert M Nosofsky,et al.  Categorization and recognition performance of a memory-impaired group: Evidence for single-system models , 2003, Journal of the International Neuropsychological Society.

[75]  Christopher Jarrold,et al.  Working Memory and the Hippocampus , 2011, Journal of Cognitive Neuroscience.

[76]  M. Packard,et al.  Amygdala Is Critical for Stress-Induced Modulation of Hippocampal Long-Term Potentiation and Learning , 2001, The Journal of Neuroscience.

[77]  Todd A Girard,et al.  Selective deficit in spatial memory strategies contrast to intact response strategies in patients with schizophrenia spectrum disorders tested in a virtual navigation task , 2013, Hippocampus.

[78]  B. Gallhofer,et al.  Hippocampal involvement in working memory encoding of changing locations: An fMRI study , 2010, Brain Research.

[79]  W. N. Schoenfeld,et al.  Principles of Psychology , 2007 .

[80]  Arthur P. Shimamura,et al.  What is the role of frontal lobe damage in memory disorders , 1991 .

[81]  F M Miezin,et al.  Activation of the hippocampus in normal humans: a functional anatomical study of memory. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[82]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[83]  Larry R Squire,et al.  Memory and Brain Systems: 1969–2009 , 2009, The Journal of Neuroscience.

[84]  J. Greig An Outline of Psychology , 1924, Nature.

[85]  C. Olson,et al.  Repetition suppression in monkey inferotemporal cortex: relation to behavioral priming. , 2007, Journal of neurophysiology.

[86]  Paul J. Reber,et al.  Neural correlates of contextual cueing are modulated by explicit learning , 2011, Neuropsychologia.

[87]  R. Clark,et al.  Classical conditioning and brain systems: the role of awareness. , 1998, Science.

[88]  A. Dickinson Actions and habits: the development of behavioural autonomy , 1985 .

[89]  Ramona O Hopkins,et al.  Working Memory and the Organization of Brain Systems , 2008, The Journal of Neuroscience.

[90]  M. D’Esposito,et al.  Medial Temporal Lobe Activity Associated with Active Maintenance of Novel Information , 2001, Neuron.

[91]  C. Gilbert,et al.  Top-down influences on visual processing , 2013, Nature Reviews Neuroscience.

[92]  A K OMMAYA,et al.  MEMORY AND THE HIPPOCAMPAL COMPLEX. , 1964, Archives of neurology.

[93]  D. Kumaran,et al.  It's In My Eyes, but It Doesn't Look that Way to Me , 2009, Neuron.

[94]  Véronique D Bohbot,et al.  Decreased functional magnetic resonance imaging activity in the hippocampus in favor of the caudate nucleus in older adults tested in a virtual navigation task , 2013, Hippocampus.

[95]  Neal J. Cohen,et al.  Short-term retention of relational memory in amnesia revisited: accurate performance depends on hippocampal integrity , 2014, Front. Hum. Neurosci..

[96]  D. Lovinger,et al.  Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill , 2009, Nature Neuroscience.

[97]  E. Tulving Episodic Memory and Autonoesis: Uniquely Human? , 2005 .

[98]  L. Squire,et al.  Intact Priming for Novel Perceptual Representations in Amnesia , 1997, Journal of Cognitive Neuroscience.

[99]  L. Squire,et al.  The medial temporal lobe memory system , 1991, Science.

[100]  Neal J. Cohen,et al.  The Long and the Short of It: Relational Memory Impairments in Amnesia, Even at Short Lags , 2006, The Journal of Neuroscience.

[101]  Safa R. Zaki,et al.  Is categorization performance really intact in amnesia? A meta-analysis , 2004, Psychonomic bulletin & review.

[102]  L. Squire,et al.  Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. , 1980, Science.

[103]  B. Staresina,et al.  Perirhinal and Parahippocampal Cortices Differentially Contribute to Later Recollection of Object- and Scene-Related Event Details , 2011, The Journal of Neuroscience.

[104]  Jan Theeuwes,et al.  Feature-based attention: it is all bottom-up priming , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[105]  R. Clark,et al.  Single-cue delay eyeblink conditioning is unrelated to awareness , 2001, Cognitive, affective & behavioral neuroscience.

[106]  D. Schacter,et al.  Reductions in cortical activity during priming , 2007, Current Opinion in Neurobiology.

[107]  Richard F. Thompson,et al.  The role of the cerebellum in classical conditioning of discrete behavioral responses , 2009, Neuroscience.

[108]  L. Squire,et al.  Experience-Dependent Eye Movements Reflect Hippocampus-Dependent (Aware) Memory , 2008, The Journal of Neuroscience.

[109]  Michael X. Cohen,et al.  Working Memory Maintenance Contributes to Long-term Memory Formation: Neural and Behavioral Evidence , 2005, Journal of Cognitive Neuroscience.

[110]  Neal J. Cohen,et al.  Observing Degradation of Visual Representations over Short Intervals When Medial Temporal Lobe Is Damaged , 2011, Journal of Cognitive Neuroscience.

[111]  R. Passingham The hippocampus as a cognitive map J. O'Keefe & L. Nadel, Oxford University Press, Oxford (1978). 570 pp., £25.00 , 1979, Neuroscience.

[112]  R. Hirsh The hippocampus and contextual retrieval of information from memory: a theory. , 1974, Behavioral biology.

[113]  M. Gluck,et al.  Intact delay-eyeblink classical conditioning in amnesia. , 1995, Behavioral neuroscience.

[114]  M. Packard,et al.  Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[115]  Charan Ranganath,et al.  Opinion TRENDS in Cognitive Sciences Vol.9 No.8 August 2005 Doubts about double dissociations between short- and long-term memory , 2022 .

[116]  L. Squire,et al.  Working memory, long-term memory, and medial temporal lobe function. , 2011, Learning & memory.

[117]  B. Postle Working memory as an emergent property of the mind and brain , 2006, Neuroscience.

[118]  Joseph E LeDoux Coming to terms with fear , 2014, Proceedings of the National Academy of Sciences.

[119]  L. Squire,et al.  The cognitive neuroscience of human memory since H.M. , 2011, Annual review of neuroscience.

[120]  D. Drachman,et al.  Memory and the hippocampal complex. II. Is memory a multiple process , 1966 .

[121]  K. Henke A model for memory systems based on processing modes rather than consciousness , 2010, Nature Reviews Neuroscience.

[122]  Deborah E. Hannula,et al.  The hippocampus reevaluated in unconscious learning and memory: at a tipping point? , 2012, Front. Hum. Neurosci..

[123]  R. Buckner,et al.  Evidence for Neural Effects of Repetition that Directly Correlate with Behavioral Priming , 2004, Journal of Cognitive Neuroscience.

[124]  Ramona O Hopkins,et al.  The role of the hippocampus in retaining relational information across short delays: the importance of memory load. , 2011, Learning & memory.

[125]  Michael Davis,et al.  NMDA receptors and fear extinction: implications for cognitive behavioral therapy , 2011, Dialogues in clinical neuroscience.

[126]  J. O'Doherty,et al.  Contributions of the striatum to learning, motivation, and performance: an associative account , 2012, Trends in Cognitive Sciences.

[127]  D. Schacter,et al.  The Evolution of Multiple Memory Systems , 1987 .

[128]  Neal J Cohen,et al.  Hiding in plain view: Lesions of the medial temporal lobe impair online representation , 2012, Hippocampus.

[129]  Ken A. Paller,et al.  Neural Manifestations of Memory with and without Awareness , 2003, Neuron.

[130]  W. Mcdougall,et al.  An Outline of Psychology , 1923 .

[131]  R. Desimone,et al.  Neural mechanisms for visual memory and their role in attention. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[132]  Deborah E. Hannula,et al.  The Eyes Have It: Hippocampal Activity Predicts Expression of Memory in Eye Movements , 2009, Neuron.

[133]  John D E Gabrieli,et al.  Working memory and long‐term memory for faces: Evidence from fMRI and global amnesia for involvement of the medial temporal lobes , 2006, Hippocampus.

[134]  Ingrid R. Olson,et al.  Working Memory for Conjunctions Relies on the Medial Temporal Lobe , 2006, The Journal of Neuroscience.

[135]  M. Petrides,et al.  Cognitive Strategies Dependent on the Hippocampus and Caudate Nucleus in Human Navigation: Variability and Change with Practice , 2003, The Journal of Neuroscience.

[136]  R. Adolphs,et al.  Double dissociation of conditioning and declarative knowledge relative to the amygdala and hippocampus in humans , 1995, Science.

[137]  H. Yin,et al.  The role of the basal ganglia in habit formation , 2006, Nature Reviews Neuroscience.

[138]  Joseph R. Manns,et al.  PSYCHOLOGICAL SCIENCE Research Article TRACE AND DELAY EYEBLINK CONDITIONING: Contrasting Phenomena of Declarative and Nondeclarative Memory , 2022 .

[139]  R. Poldrack,et al.  Characterizing the neural mechanisms of skill learning and repetition priming: evidence from mirror reading. , 2001, Brain : a journal of neurology.

[140]  Russell A Poldrack,et al.  Sequence Learning What's the Hippocampus to Do? , 2003, Neuron.

[141]  Larry R Squire,et al.  Contrasting effects on path integration after hippocampal damage in humans and rats , 2013, Proceedings of the National Academy of Sciences.

[142]  Terry Winograd,et al.  FRAME REPRESENTATIONS AND THE DECLARATIVE/PROCEDURAL CONTROVERSY , 1975 .

[143]  Maarten Speekenbrink,et al.  Models of recognition, repetition priming, and fluency: exploring a new framework. , 2012, Psychological review.

[144]  A. Graybiel,et al.  Differential Dynamics of Activity Changes in Dorsolateral and Dorsomedial Striatal Loops during Learning , 2010, Neuron.