Opinion | Published:

A model for memory systems based on processing modes rather than consciousness

Nature Reviews Neuroscience volume 11, pages 523532 (2010) | Download Citation

Abstract

Prominent models of human long-term memory distinguish between memory systems on the basis of whether learning and retrieval occur consciously or unconsciously. Episodic memory formation requires the rapid encoding of associations between different aspects of an event which, according to these models, depends on the hippocampus and on consciousness. However, recent evidence indicates that the hippocampus mediates rapid associative learning with and without consciousness in humans and animals, for long-term and short-term retention. Consciousness seems to be a poor criterion for differentiating between declarative (or explicit) and nondeclarative (or implicit) types of memory. A new model is therefore required in which memory systems are distinguished based on the processing operations involved rather than by consciousness.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    Memory and Brain (Oxford Univ. Press, New York, 1987).

  2. 2.

    Memory and the hippocampus — a synthesis from findings with rats, monkeys, and humans. Psychol. Rev. 99, 195–231 (1992).

  3. 3.

    & Implicit and explicit memory for new associations in normal and amnesic subjects. J. Exp. Psychol. Learn. Mem. Cogn. 11, 501–518 (1985).

  4. 4.

    Cognitive neuroscience of human memory. Annu. Rev. Psychol. 49, 87–115 (1998).

  5. 5.

    Recovered consciousness — a hypothesis concerning modularity and episodic memory. J. Clin. Exp. Neuropsychol. 17, 276–290 (1995).

  6. 6.

    & Memory, Amnesia, and the Hippocampal System (MIT Press, Cambridge, Massachusetts, 1993).

  7. 7.

    & Implicit learning: below the subjective threshold. Psychon. Bull. Rev. 4, 3–23 (1997).

  8. 8.

    Direct efferent and afferent connections of the hippocampus with the neocortex in the marmoset monkey. Am. J. Anat. 156, 77–82 (1979).

  9. 9.

    & Organization of direct hippocampal efferent projections to the cerebral cortex of the rhesus monkey: projections from CA1, prosubiculum, and subiculum to the temporal lobe. J. Comp. Neurol. 392, 92–114 (1998).

  10. 10.

    & in The Human Nervous System (eds Paxinos, G. & Mai, J. K.) 871–914 (Academic Press, San Diego, 2004).

  11. 11.

    & Computational analysis of the role of the hippocampus in memory. Hippocampus 4, 374–391 (1994).

  12. 12.

    & The hippocampal memory indexing theory. Behav. Neurosci. 100, 147–154 (1986).

  13. 13.

    & Structure and function of declarative and nondeclarative memory systems. Proc. Natl Acad. Sci. USA 93, 13515–13522 (1996).

  14. 14.

    & Configural association theory and the hippocampal formation: an appraisal and reconfiguration. Hippocampus 5, 375–389 (1995).

  15. 15.

    , & Why there are complementary learning systems in the hippocampus and neocortex — insights from the successes and failures of connectionist models of learning and memory. Psychol. Rev. 102, 419–457 (1995).

  16. 16.

    & Modeling hippocampal and neocortical contributions to recognition memory: a complementary-learning-systems approach. Psychol. Rev. 110, 611–646 (2003).

  17. 17.

    & Computational principles of learning in the neocortex and hippocampus. Hippocampus 10, 389–397 (2000).

  18. 18.

    & Electrolytic lesions of dorsal CA3 impair episodic-like memory in rats. Neurobiol. Learn. Mem. 89, 192–198 (2008).

  19. 19.

    & Long-term potentiation in the neocortex of the adult, freely moving rat. Cereb. Cortex 8, 719–729 (1998).

  20. 20.

    , & Computer learning by memory-impaired patients — acquisition and retention of complex knowledge. Neuropsychologia 24, 313–328 (1986).

  21. 21.

    , & Long-lasting perceptual priming and semantic learning in amnesia — a case experiment. J. Exp. Psychol. Learn. Mem. Cogn. 17, 595–617 (1991).

  22. 22.

    & On the implicit learning of novel associations by amnesic patients and normal subjects. Neuropsychology 7, 119–135 (1993).

  23. 23.

    , & Acquisition of post-morbid vocabulary and semantic facts in the absence of episodic memory. Brain 121, 1313–1327 (1998).

  24. 24.

    , , , & Differential involvement of the hippocampus and temporal lobe cortices in rapid and slow learning of new semantic information. Neuropsychologia 40, 748–768 (2002).

  25. 25.

    , & Evidence for semantic learning in profound amnesia: an investigation with patient HM. Hippocampus 14, 417–425 (2004).

  26. 26.

    , & Normal olfactory discrimination learning set and facilitation of reversal learning after medial temporal damage in rats — implications for an account of preserved learning abilities in amnesia. J. Neurosci. 6, 1876–1884 (1986).

  27. 27.

    , , & Hippocampal system dysfunction and odor discrimination learning in rats — impairment or facilitation depending on representational demands. Behav. Neurosci. 102, 331–339 (1988).

  28. 28.

    , & Further studies of hippocampal representation during odor discrimination learning. Behav. Neurosci. 103, 1207–1216 (1989).

  29. 29.

    , , & Damage to the hippocampal formation in rats selectively impairs the ability to learn cue relationships. Behav. Neural Biol. 52, 331–356 (1989).

  30. 30.

    & Conservation of hippocampal memory function in rats and humans. Nature 379, 255–257 (1996).

  31. 31.

    , & Transitivity, flexibility, conjunctive representations, and the hippocampus. II. A computational analysis. Hippocampus 13, 341–354 (2003).

  32. 32.

    & The hippocampus and memory for 'what', 'where' and 'when' Learn. Mem. 11, 397–405 (2004).

  33. 33.

    , & Can animals recall the past and plan for the future? Nature Rev. Neurosci. 4, 685–691 (2003).

  34. 34.

    Episodic memory: from mind to brain. Annu. Rev. Psychol. 53, 1–25 (2002).

  35. 35.

    Episodic memory and common sense: how far apart? Phil. Trans. R. Soc. Lond. B 356, 1505–1515 (2001).

  36. 36.

    & Behavioural evidence for mental time travel in nonhuman animals. Behav. Brain Res. 03 Dec 2009 (doi: 10.1016/j.bbr.2009.11.044).

  37. 37.

    & Episodic-like memory during cache recovery by scrub jays. Nature 395, 272–274 (1998).

  38. 38.

    & Amnesia — a disconnection syndrome. Neuropsychologia 20, 233–248 (1982).

  39. 39.

    , , , & Relative sparing of item recognition memory in a patient with adult-onset damage limited to the hippocampus. Hippocampus 12, 325–340 (2002).

  40. 40.

    et al. Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition. Hippocampus 14, 763–784 (2004).

  41. 41.

    & Interleaving brain systems for episodic and recognition memory. Trends Cogn. Sci. 10, 455–463 (2006).

  42. 42.

    The nature of recollection and familiarity: a review of 30 years of research. J. Mem. Lang. 46, 441–517 (2002).

  43. 43.

    , & Intra- and inter-item associations doubly dissociate the electrophysiological correlates of familiarity and recollection. Neuron 52, 535–545 (2006).

  44. 44.

    , & Effect of unitization on associative recognition in amnesia. Hippocampus 17, 192–200 (2007).

  45. 45.

    , , & Perirhinal cortex supports encoding and familiarity-based recognition of novel associations. Neuron 59, 554–560 (2008).

  46. 46.

    , & Disproportionate deficit in associative recognition relative to item recognition in global amnesia. Cogn. Affect. Behav. Neurosci. 3, 186–194 (2003).

  47. 47.

    , , , & Role of the medial temporal lobes in relational memory: neuropsychological evidence from a cued recognition paradigm. Neuropsychologia 45, 2589–2597 (2007).

  48. 48.

    & Acquisition and transfer of new verbal information in amnesia: retrieval and neuroanatomical constraints. Neuropsychology 14, 427–455 (2000).

  49. 49.

    , , & Amnesia is a deficit in relational memory. Psychol. Sci. 11, 454–461 (2000).

  50. 50.

    , , , & Implicit memory for novel conceptual associations in amnesia. Cogn. Affect. Behav. Neurosci. 6, 91–101 (2006).

  51. 51.

    , , & Rapid onset relational memory effects are evident in eye movement behavior, but not in hippocampal amnesia. J. Cogn. Neurosci. 19, 1690–1705 (2007).

  52. 52.

    , , & Development of shared information in communication despite hippocampal amnesia. Nature Neurosci. 9, 140–146 (2006).

  53. 53.

    & Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage. Nature Neurosci. 2, 844–847 (1999).

  54. 54.

    , , & The effect of midazolam on visual search: implications for understanding amnesia. Proc. Natl Acad. Sci. USA 101, 17879–17883 (2004).

  55. 55.

    , , & Hippocampal differentiation without recognition: an fMRI analysis of the contextual cueing task. Learn. Mem. 14, 548–553 (2007).

  56. 56.

    & Perceptual learning, awareness, and the hippocampus. Hippocampus 11, 776–782 (2001).

  57. 57.

    & Dissociation between explicit memory and configural memory in the human medial temporal lobe. Cereb. Cortex 18, 2192–2207 (2008).

  58. 58.

    et al. Associative encoding of pictures activates the medial temporal lobes. Hum. Brain Mapp. 6, 85–104 (1998).

  59. 59.

    & Mind the gap: binding experiences across space and time in the human hippocampus. Neuron 63, 267–276 (2009).

  60. 60.

    & Does hippocampus associate discontiguous events? — Evidence from event-related fMRI. Hippocampus 15, 141–148 (2005).

  61. 61.

    et al. Probing the transformation of discontinuous associations into episodic memory: an event-related fMRI study. Neuroimage 38, 212–222 (2007).

  62. 62.

    , & Time-dependent changes in learning audiovisual associations: a single-trial fMRI study. Neuroimage 11, 243–255 (2000).

  63. 63.

    , , & Human hippocampus establishes associations in memory. Hippocampus 7, 249–256 (1997).

  64. 64.

    , , , & Human hippocampus associates information in memory. Proc. Natl Acad. Sci. USA 96, 5884–5889 (1999).

  65. 65.

    et al. Visual association encoding activates the medial temporal lobe: a functional magnetic resonance imaging study. Hippocampus 7, 594–601 (1997).

  66. 66.

    & The eyes have it: hippocampal activity predicts expression of memory in eye movements. Neuron 63, 592–599 (2009).

  67. 67.

    et al. Nonconscious formation and reactivation of semantic associations by way of the medial temporal lobe. Neuropsychologia 41, 863–876 (2003).

  68. 68.

    et al. Active hippocampus during nonconscious memories. Conscious. Cogn. 12, 31–48 (2003).

  69. 69.

    et al. Implicit associative learning engages the hippocampus and interacts with explicit associative learning. Neuron 46, 505–520 (2005).

  70. 70.

    , & Further analysis of hippocampal amnesic syndrome — 14-year follow-up study of H. M. Neuropsychologia 6, 215–234 (1968).

  71. 71.

    , , & Similarities and differences in the neural correlates of episodic memory retrieval and working memory. Neuroimage 16, 317–330 (2002).

  72. 72.

    , , & Working memory and long-term memory for faces: evidence from fMRI and global amnesia for involvement of the medial temporal lobes. Hippocampus 16, 604–616 (2006).

  73. 73.

    & Medial temporal lobe activity associated with active maintenance of novel information. Neuron 31, 865–873 (2001).

  74. 74.

    et al. Sustained neural activity patterns during working memory in the human medial temporal lobe. J. Neurosci. 27, 7807–7816 (2007).

  75. 75.

    , & Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load. Cereb. Cortex 18, 1618–1629 (2008).

  76. 76.

    , & The long and the short of it: relational memory impairments in amnesia, even at short lags. J. Neurosci. 26, 8352–8359 (2006).

  77. 77.

    , , , & Working memory for conjunctions relies on the medial temporal lobe. J. Neurosci. 26, 4596–4601 (2006).

  78. 78.

    & Doubts about double dissociations between short- and long-term memory. Trends Cogn. Sci. 9, 374–380 (2005).

  79. 79.

    , , & Implicit working memory. Conscious. Cogn. 18, 665–678 (2009).

  80. 80.

    , & Levels of processing versus transfer appropriate processing. J. Verb. Learn. Verb. Behav. 16, 519–533 (1977).

  81. 81.

    Investigating dissociations among memory measures — support for a transfer-appropriate processing framework. J. Exp. Psychol. Learn. Mem. Cogn. 15, 657–668 (1989).

  82. 82.

    Perceptual representation systems and implicit memory — toward a resolution of the multiple memory-systems debate. Ann. NY Acad. Sci. 608, 543–571 (1990).

  83. 83.

    & The hippocampus and memory: insights from spatial processing. Nature Rev. Neurosci. 9, 182–194 (2008).

  84. 84.

    Pavlovian fear conditioning as a behavioral assay for hippocampus and amygdala function: cautions and caveats. Eur. J. Neurosci. 28, 1661–1666 (2008).

  85. 85.

    & Hippocampal involvement in contextual modulation of fear extinction. Hippocampus 17, 749–758 (2007).

  86. 86.

    & Retrograde amnesia and memory consolidation — a neurobiological perspective. Curr. Opin. Neurobiol. 5, 169–177 (1995).

  87. 87.

    et al. Functional neuroanatomy of remote episodic, semantic and spatial memory: a unified account based on multiple trace theory. J. Anat. 207, 35–66 (2005).

  88. 88.

    in The Neuropsychology of Memory (eds Squire, L. R. & Butters, N.) 52–62 (Guilford Press, New York, 1984).

  89. 89.

    , , & Differential contribution of dorsal and ventral hippocampus to trace and delay fear conditioning. Hippocampus 19, 33–44 (2009).

  90. 90.

    Integrating associative learning signals across the brain. Hippocampus 17, 842–850 (2007).

  91. 91.

    et al. Interactive memory systems in the human brain. Nature 414, 546–550 (2001).

  92. 92.

    , , & An fMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 37, 1013–1025 (2003).

  93. 93.

    et al. Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 58, 261–272 (2008).

  94. 94.

    & Classical conditioning and brain systems: the role of awareness. Science 280, 77–81 (1998).

  95. 95.

    , & Specificity of priming: a cognitive neuroscience perspective. Nature Rev. Neurosci. 5, 853–862 (2004).

  96. 96.

    & Recognition memory: neuronal substrates of the judgement of prior occurrence. Prog. Neurobiol. 55, 149–189 (1998).

  97. 97.

    , , & Lag-sensitive repetition suppression effects in the anterior parahippocampal gyrus. Hippocampus 15, 557–561 (2005).

  98. 98.

    & An illusion of memory — false recognition influenced by unconscious perception. J. Exp. Psychol. Gen. 118, 126–135 (1989).

  99. 99.

    , & Contribution of perceptual fluency to recognition judgments. J. Exp. Psychol. Learn. Mem. Cogn. 17, 210–223 (1991).

  100. 100.

    , & Accurate forced-choice recognition without awareness of memory retrieval. Learn. Mem. 15, 454–459 (2008).

  101. 101.

    , , & The neural system that mediates familiarity memory. Hippocampus 16, 504–520 (2006).

  102. 102.

    et al. Impaired familiarity with preserved recollection after anterior temporal-lobe resection that spares the hippocampus. Proc. Natl Acad. Sci. USA 104, 16382–16387 (2007).

  103. 103.

    , & Establishing a relationship between activity reduction in human perirhinal cortex and priming. Hippocampus 19, 773–778 (2009).

  104. 104.

    & Intact perceptual memory in the absence of conscious memory. Behav. Neurosci. 111, 850–854 (1997).

  105. 105.

    & Recognition memory and familiarity judgments in severe amnesia: no evidence for a contribution of repetition priming. Behav. Neurosci. 114, 459–467 (2000).

  106. 106.

    , & Conceptual priming and familiarity: different expressions of memory during recognition testing with distinct neurophysiological correlates. J. Cogn. Neurosci. 24 Aug 2009 (doi: 10.1162/jocn.2009.21341)

  107. 107.

    , , , & A familiarity signal in human anterior medial temporal cortex? Hippocampus 13, 301–304 (2003).

  108. 108.

    , & The role of explicit memory processes in cross-modal priming: an investigation of stem completion priming in amnesia. Cogn. Affect. Behav. Neurosci. 1, 222–228 (2001).

  109. 109.

    , , & Functional MRI evidence for a role of frontal and inferior temporal cortex in amodal components of priming. Brain 123, 620–640 (2000).

  110. 110.

    et al. Brain activity during intra- and cross-modal priming: new empirical data and review of the literature. Neuropsychologia 42, 14–24 (2004).

  111. 111.

    & Implicit memory for phonological processes in visual stem completion. Mem. Cognit. 27, 1–11 (1999).

  112. 112.

    & Imaging cognition II: an empirical review of 275 PET and fMRI studies. J. Cogn. Neurosci. 12, 1–47 (2000).

  113. 113.

    , & “I remember it as if it were yesterday”: memory for recent events in patients with semantic dementia. Neuropsychologia 47, 1344–1351 (2009).

  114. 114.

    , , , & Face–name repetition priming in semantic dementia: a case report. Brain Cogn. 70, 231–237 (2009).

  115. 115.

    , & Consciousness in congenitally decorticate children: developmental vegetative state as self-fulfilling prophecy. Dev. Med. Child Neurol. 41, 364–374 (1999).

  116. 116.

    & Evaluating the neuropsychological dissociation evidence for multiple memory systems. Cogn. Affect. Behav. Neurosci. 3, 168–185 (2003).

  117. 117.

    The hippocampus as a 'stupid', domain-specific module: implications for theories of recent and remote memory, and of imagination. Can. J. Exp. Psychol. 62, 62–79 (2008).

  118. 118.

    & A comparison and evaluation of the predictions of relational and conjunctive accounts of hippocampal function. Hippocampus 16, 43–65 (2006).

  119. 119.

    , , & Dynamics of the hippocampus during encoding and retrieval of face–name pairs. Science 299, 577–580 (2003).

  120. 120.

    , & Dissociable properties of memory systems: differences in the flexibility of declarative and nondeclarative knowledge. Behav. Neurosci. 110, 861–871 (1996).

  121. 121.

    , , , & The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23, 209–226 (1999).

  122. 122.

    , & The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30, 123–152 (2007).

  123. 123.

    , & Memory systems do not divide on consciousness: reinterpreting memory in terms of activation and binding. Psychol. Bull. 135, 23–49 (2009).

  124. 124.

    et al. Converging intracranial markers of conscious access. PLoS Biol. 7, 472–492 (2009).

  125. 125.

    & Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition 79, 1–37 (2001).

  126. 126.

    Acquisition of motor skill after bilateral medial temporal-lobe excision. Neuropsychologia 6, 255–265 (1968).

  127. 127.

    & What can amnesic patients learn. Neuropsychologia 14, 111–122 (1976).

  128. 128.

    & New method of testing long-term retention with special reference to amnesic patients. Nature 217, 972–974 (1968).

  129. 129.

    & Preserved learning and retention of pattern-analyzing skill in amnesia — dissociation of knowing how and knowing that. Science 210, 207–210 (1980).

  130. 130.

    & The learning of categories — parallel brain systems for item memory and category knowledge. Science 262, 1747–1749 (1993).

  131. 131.

    , & The information that amnesic patients do not forget. J. Exp. Psychol. Learn. Mem. Cogn. 10, 164–178 (1984).

  132. 132.

    , & Intact conceptual priming in the absence of declarative memory. Psychol. Sci. 15, 680–686 (2004).

  133. 133.

    & Conditioning in amnesic patients. Neuropsychologia 17, 187–194 (1979).

  134. 134.

    , & Intact artificial grammar learning in amnesia — dissociation of classification learning and explicit memory for specific instances. Psychol. Sci. 3, 172–179 (1992).

  135. 135.

    , & Memory as assessed by recognition and reading time in normal and memory-impaired people with Alzheimers-disease and other neurological disorders. J. Exp. Psychol. Gen. 115, 331–347 (1986).

  136. 136.

    , & Intact implicit memory for newly formed verbal associations in amnesic patients following single study trials. Neuropsychology 14, 570–578 (2000).

  137. 137.

    , , & Preservation of implicit memory for new associations in global amnesia. Psychol. Sci. 8, 326–329 (1997).

  138. 138.

    & Preserved learning in amnesic patients — perspectives from research on direct priming. J. Clin. Exp. Neuropsychol. 8, 727–743 (1986).

  139. 139.

    & Impaired priming of new associations in amnesia. J. Exp. Psychol. Learn. Mem. Cogn. 15, 721–728 (1989).

  140. 140.

    & Implicit memory and test awareness. J. Exp. Psychol. Learn. Mem. Cogn. 16, 404–416 (1990).

  141. 141.

    & Explicit contamination in 'implicit' memory for new associations. Mem. Cognit. 25, 352–366 (1997).

  142. 142.

    Memory and awareness. Science 280, 59–60 (1998).

  143. 143.

    Memory and consciousness. Can. Psychol. 26, 1–12 (1985).

  144. 144.

    & Unbiased stereological estimation of the number of neurons in the human hippocampus. J. Comp. Neurol. 296, 1–22 (1990).

  145. 145.

    , & Organization of intrahippocampal projections originating from CA3 pyramidal cells in the rat. J. Comp. Neurol. 295, 580–623 (1990).

Download references

Acknowledgements

The author would like to thank T. Reber, O. Markes, B. Meier and S. Duss for valuable help and discussions. K.H. is supported by Swiss National Science Foundation Grants 320000-114012 and K-13K1-119953.

Author information

Affiliations

  1. Katharina Henke is at the Department of Psychology, University of Bern, Muesmattstrasse 45, 3000 Bern 9, Switzerland.  henke@psy.unibe.ch

    • Katharina Henke

Authors

  1. Search for Katharina Henke in:

Competing interests

The author declares no competing financial interests.

About this article

Publication history

Published

DOI

https://doi.org/10.1038/nrn2850

Further reading