Exploration of the Neurobiological Basis for a Three-System, Multi-attribute Model of Memory

  • Raymond P. KesnerEmail author


The structure and utilization of memory is central to one’s knowledge of the past, interpretation of the present, and prediction of the future. Therefore, the understanding of the structural and process components of memory systems at the psychological and neurobiological level is of paramount importance. In this chapter, I am presenting data in support of a neurobiological basis for an attribute model based on different forms or attributes of memory such as space, time, response, sensory-perception, reward value (affect) and in humans a language attribute is also added. These attributes are processed by different neural regions and interconnected networks across all three (event-based, knowledge-based, and rule-based) memory systems. Each memory system operates in processing mnemonic information based on a unique set of processes. The selection of some of these processes has been influenced greatly by computational models of specific brain regions. For each brain area there are a large number of processes that define the operation of each memory system. The hippocampus is used extensively, but not exclusively, to detail the multiple operations that characterize the overall activity of this brain region within the event-based memory system. The processes that are discussed for the event-based memory system include conjunctive encoding, spatial pattern separation, formation of arbitrary associations, pattern completion, and temporal pattern separation. The processes that are discussed for the knowledge-based memory system include perceptual memory and repetition priming. For the rule-based memory system the process of working memory is presented. Furthermore, based on brain-behavior experiments, there are interactions and parallel processing operations between the event-based memory system and the knowledge-based systems, between the event-based and rule-based memory systems, and between the rule-based and knowledge-based systems.


Event-based memory Knowledge-based memory Rule-based memory Neural substrates of memory Conjunctive encoding Spatial pattern separation Arbitrary associations Pattern completion Temporal pattern separation Perceptual memory 


  1. Bussey, T. J., Muir, J. L., Everitt, B. J., & Robbins, T. W. (1996). Dissociable effects of anterior and posterior cingulate cortex lesions on the acquisition of a conditional visual discrimination: Facilitation of early learning vs. impairment of late learning. Behavioural Brain Research, 82, 45–56.PubMedCrossRefGoogle Scholar
  2. Bussey, T. J., Muir, J. L., Everitt, B. J., & Robbins, T. W. (1997). Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. Behavioral Neuroscience, 111, 920–936.PubMedCrossRefGoogle Scholar
  3. Chiba, A. A., Kesner, R. P., & Reynolds, A. M. (1994). Memory for spatial location as a function of temporal lag in rats: Role of hippocampus and medial prefrontal cortex. Behavioral and Neural Biology, 61, 123–131.PubMedCrossRefGoogle Scholar
  4. Chiba, A. A., Kesner, R. P., & Gibson, C. J. (1997). Memory for temporal order of new and familiar spatial location sequences: Role of the medial prefrontal cortex. Learning and Memory, 4, 311–317.PubMedCrossRefGoogle Scholar
  5. Chiba, A. A., Kesner, R. P., & Jackson, P. (2002). Two forms of spatial memory: A double ­dissociation between the parietal cortex and the hippocampus in the rat. Behavioral Neuroscience, 116, 874–883.PubMedCrossRefGoogle Scholar
  6. Cho, Y. H., & Kesner, R. P. (1996). Involvement of entorhinal cortex or parietal cortex in long-term spatial discrimination memory in rats: Retrograde amnesia. Behavioral Neuroscience, 110, 436–442.PubMedCrossRefGoogle Scholar
  7. Cho, Y. H., Kesner, R. P., & Brodale, S. (1995). Retrograde and anterograde amnesia for spatial discrimination in rats: Role of hippocampus, entorhinal cortex and parietal cortex. Psychobiology, 23, 185–194.Google Scholar
  8. Churchwell, J. C., & Kesner, R. P. (2011). Hippocampal-prefrontal dynamics in spatial working memory: Interactions and independent parallel processing. Behavioural Brain Research, 225, 389–395.PubMedCentralPubMedCrossRefGoogle Scholar
  9. Cohen, N. J., & Eichenbaum, H. B. (1993). Memory, amnesia, and hippocampal function. ­Cambridge: MIT Press.Google Scholar
  10. Corwin, J. V., Fussinger, M., Meyer, R. C., King, V. R., & Reep, R. L. (1994). Bilateral destruction of the ventrolateral orbital cortex produces allocentric but not egocentric spatial deficits in rats. Behavioural Brain Research, 61, 79–86.PubMedCrossRefGoogle Scholar
  11. Day, M., Langston, R., & Morris, R. G. (2003). Glutamate-receptor-mediated encoding and ­retrieval of paired-associate learning. Nature, 424, 205–209.PubMedCrossRefGoogle Scholar
  12. deBruin, J. P. C., Swinkels, W. A. M., & deBrabander, J. M. (1997). Response learning of rats in a Morris water maze: Involvement of the medial prefrontal cortex. Behavioural Brain Research, 85, 47–55.CrossRefGoogle Scholar
  13. DeCoteau, W. E., & Kesner, R. P. (1998). Effects of hippocampal and parietal cortex lesions on the processing of multiple object scenes. Behavioral Neuroscience, 112, 68–82.PubMedCrossRefGoogle Scholar
  14. DeCoteau, W. E., Kesner, R. P., & Williams, J. M. (1997). Short-term memory for food reward magnitude: The role of the prefrontal cortex. Behavioural Brain Research, 88, 239–249.PubMedCrossRefGoogle Scholar
  15. Delatour, B., & Gisquet-Verrier, P. (1996). Prelimbic cortex specific lesions disrupt delayed ­variable response tasks in the rat. Behavioral Neuroscience, 110, 1282–1298.PubMedCrossRefGoogle Scholar
  16. DiMattia, B. V., & Kesner, R. P. (1988). Spatial cognitive maps: Differential role of parietal cortex and hippocampal formation. Behavioral Neuroscience, 102, 471–480.PubMedCrossRefGoogle Scholar
  17. Eichenbaum, H. (1994). The hippocampal system and declarative memory in humans and animals: Experimental analysis and historical origins. In D. L. Schacter & E. Tulving (Eds.), Memory systems 1994 (pp. 39–63). Cambridge: MIT Press.Google Scholar
  18. Eichenbaum, H. (2004). Hippocampus: Cognitive processes and neural representation that ­underlie declarative memory. Neuron, 44, 109–120.PubMedCrossRefGoogle Scholar
  19. Eichenbaum, H., Clegg, R. A., & Feeley, A. (1983). Reexamination of functional subdivisions of the rodent prefrontal cortex. Experimental Neurology, 79, 434–451.PubMedCrossRefGoogle Scholar
  20. Ennaceur, A., Neave, N., & Aggleton, J. P. (1997). Spontaneous object recognition and object location memory in rats: The effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix. Experimental Brain Research, 113, 509–519.PubMedCrossRefGoogle Scholar
  21. Estes, W. K. (1986). Memory for temporal information. In J. A. Michon & J. L. Jackson (Eds.), Time, mind and behavior (pp. 151–168). New York: Springer.Google Scholar
  22. Ferbinteanu, J., Holsinger, R. M., & McDonald, R. J. (1999). Lesions of the medial or lateral perforant path have different effects on hippocampal contributions to place learning and fear conditioning to context. Behavioural Brain Research, 101, 65–84.PubMedCrossRefGoogle Scholar
  23. Foreman, N., Save, E., Thinus-Blanc, C., & Buhot, M. C. (1992). Visually guided locomotion, distractibility, and the missing-stimulus effect in hooded rates with unilateral or bilateral lesions of parietal cortex. Behavioral Neuroscience, 106, 529–538.PubMedCrossRefGoogle Scholar
  24. Gilbert, P. E., & Kesner, R. P. (2002a). The amygdala but not the hippocampus is involved in ­pattern separation based on reward value. Neurobiology of Learning and Memory, 77, 338–353.PubMedCrossRefGoogle Scholar
  25. Gilbert, P. E., & Kesner, R. P. (2002b). Role of the rodent hippocampus in paired-associate learning involving associations between a stimulus and a spatial location. Behavioral Neuroscience, 116, 63–71.PubMedCrossRefGoogle Scholar
  26. Gilbert, P. E., & Kesner, R. P. (2003a). Recognition memory for complex visual discrimination is influenced by stimulus interference in rodents with perirhinal cortex damage. Learning & Memory, 10, 525–530.CrossRefGoogle Scholar
  27. Gilbert, P. E., & Kesner, R. P. (2003b). Localization of function within the dorsal hippocampus: The role of the CA3 subregion in paired-associate learning. Behavioral Neuroscience, 117, 1385–1394.PubMedCrossRefGoogle Scholar
  28. Gilbert, P. E., & Kesner, R. P. (2006). The role of dorsal CA3 hippocampal subregion in spatial working memory and pattern separation. Behavioural Brain Research, 169, 142–149.PubMedCrossRefGoogle Scholar
  29. Gilbert, P. E., Kesner, R. P., & Lee, I. (2001). Dissociating hippocampal subregions: A double ­dissociation between dentate gyrus and CA1. Hippocampus, 11, 626–636.PubMedCrossRefGoogle Scholar
  30. Gold, E., & Kesner, R. P. (2005). The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus, 15, 808–814.PubMedCrossRefGoogle Scholar
  31. Hafting, T., Fyhn, M., Molden, S., Moser, M. B., & Moser, E. I. (2005). Microstructure of a spatial map in the entorhinal cortex. Nature, 436, 801–806.PubMedCrossRefGoogle Scholar
  32. Hargreaves, E. L., Rao, G., Lee, I., & Knierim, J. J. (2005). Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science, 308, 1792–1794.PubMedCrossRefGoogle Scholar
  33. Harrison, L. D., & Mair, R. G. (1996). A comparison of the effects of frontal cortical and thalamic lesions on measures of spatial learning and memory in the rat. Behavioural Brain Research, 75, 195–206.PubMedCrossRefGoogle Scholar
  34. Hasselmo, M. E., & Wyble, B. P. (1997). Free recall and recognition in a network model of the hippocampus: Simulating effects of scopolamine on human memory function. Behavioural Brain Research, 89, 1–34.PubMedCrossRefGoogle Scholar
  35. Ho, J. W., Narduzzo, K. E., Outram, A., Tinsley, C. J., Henley, J. M., Warburton, E. C., & Brown, M. W. (2011). Contributions of areaTe2 to rat recognition memory. Learning and Memory, 18, 493–501.Google Scholar
  36. Hunsaker, M. R., Mooy, G. G., Swift, J. S., & Kesner, R. P. (2007). Dissociations of the medial and lateral perforant path projections into dorsal DG, CA3, and CA1 for spatial and nonspatial (visual object) information processing. Behavioral Neuroscience, 121, 742–750.PubMedCrossRefGoogle Scholar
  37. Hunsaker, M. R., Lee, B., & Kesner, R. P. (2008). Evaluating the temporal context of episodic memory: The role of CA3 and CA1. Behavioural Brain Research, 188, 310–315.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Jackson, P. A., Kesner, R. P., & Amann, K. (1998). Memory for duration: Role of hippocampus and medial prefrontal cortex. Neurobiology of Learning and Memory, 70, 328–348.PubMedCrossRefGoogle Scholar
  39. Jay, T. M., & Witter, M. P. (1991). Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. Journal of Comparative Neurology, 313, 574–586.PubMedCrossRefGoogle Scholar
  40. Kesner, R. P. (1989). Retrospective and prospective coding of information: Role of the medial prefrontal cortex. Experimental Brain Research, 74, 163–167.PubMedCrossRefGoogle Scholar
  41. Kesner, R. P. (1990). Memory for frequency in rats: Role of the hippocampus and medial prefrontal cortex. Behavioral and Neural Biology, 53, 402–410.PubMedCrossRefGoogle Scholar
  42. Kesner, R. P. (1998a). Neural mediation of memory for time: Role of the hippocampus and medial prefrontal cortex. Psychonomic Bulletin and Review, 5, 585–596.CrossRefGoogle Scholar
  43. Kesner, R. P. (1998b). Neurobiological views of memory. In J. L. Martinez & R. P. Kesner (Eds.), The neurobiology of learning and memory (pp. 361–416). San Diego: Academic.CrossRefGoogle Scholar
  44. Kesner, R. P. (1999). Perirhinal cortex and hippocampus mediate parallel processing of object and spatial location information. Behavioural and Brain Sciences, 22, 455–479.CrossRefGoogle Scholar
  45. Kesner, R. P. (2000a). Subregional analysis of mnemonic functions of the prefrontal cortex in the rat. Psychobiology, 28, 219–228.Google Scholar
  46. Kesner, R. P. (2000b). Behavioral analysis of the contribution of the hippocampus and parietal cortex to the processing of information: Interactions and dissociations. Hippocampus, 10, 483–490.PubMedCrossRefGoogle Scholar
  47. Kesner, R. P. (2007). Neurobiological views of memory. In R. P. Kesner & J. L. Martinez (Eds.), The neurobiology of learning and memory (2nd ed., pp. 271–304). San Diego: Academic.CrossRefGoogle Scholar
  48. Kesner, R. P., & Churchwell, J. C. (2011). An analysis of rat prefrontal cortex in mediating executive function. Neurobiology of Learning and Memory, 96, 417–431.PubMedCrossRefGoogle Scholar
  49. Kesner, R. P., & Creem-Regehr, S. H. (2013). Parietal contributions to spatial cognition. In L. Nadel & D. Waller (Eds.), Handbook of spatial cognition (pp. 35–64). Washington: American Psychological Association.CrossRefGoogle Scholar
  50. Kesner, R. P., & Gilbert, P. (2006). The role of the medial caudate nucleus, but not the hippocampus, in a matching-to sample task for a motor response. The European Journal of Neuroscience, 23, 1888–1894.PubMedCrossRefGoogle Scholar
  51. Kesner, R. P., & Holbrook, T. (1987). Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia, 25, 653–664.PubMedCrossRefGoogle Scholar
  52. Kesner, R. P., & Hopkins, R. O. (2006). Mnemonic functions of the hippocampus: A comparison between animals and humans. Biological Psychology, 73, 3–18.PubMedCrossRefGoogle Scholar
  53. Kesner, R. P., & Warthen, D. K. (2010). Implications of CA3 NMDA and opiate receptors for spatial pattern completion in rats. Hippocampus, 20, 550–557.PubMedGoogle Scholar
  54. Kesner, R. P., DiMattia, B. V., & Crutcher, K. A. (1987). Evidence for neocortical involvement in reference memory. Behavioral and Neural Biology, 47, 40–53.PubMedCrossRefGoogle Scholar
  55. Kesner, R. P., Farnsworth, G., & DiMattia, B. V. (1989). Double-dissociation of egocentric and allocentric space following medial prefrontal and parietal cortex lesions in the rat. Behavioral Neuroscience, 103, 956–961.PubMedCrossRefGoogle Scholar
  56. Kesner, R. P., Fansworth, G., & Kametani, H. (1991). Role of parietal cortex and hippocampus in representing spatial information. Cerebral Cortex, 1, 367–373.PubMedCrossRefGoogle Scholar
  57. Kesner, R. P., Bolland, B., & Dakis, M. (1993). Memory for spatial locations, motor responses, and objects: Triple dissociations among the hippocampus, caudate nucleus and extrastriate visual cortex. Experimental Brain Research, 93, 462–470.PubMedCrossRefGoogle Scholar
  58. Kesner, R. P., Hunt, M. E., Williams, J. M., & Long, J. M. (1996). Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cerebral Cortex, 6, 311–318.PubMedCrossRefGoogle Scholar
  59. Kesner, R. P., Lee, I., & Gilbert, P. (2004). A behavioral assessment of hippocampal function based on a subregional analysis. Reviews in the Neuroscience, 15, 333–351.CrossRefGoogle Scholar
  60. Kesner, R. P., Hunsaker, M. R., & Warthen, M. W. (2008). The CA3 subregion of the hippocampus is critical for episodic memory processing by means of relational encoding in rats. Behavioral Neuroscience, 122, 1217–1225.PubMedCrossRefGoogle Scholar
  61. Kim, J., & Ragozzino. M. E. (2005). The involvement of the orbitofrontal cortex in learning under changing task contingencies. Neurobiology of Learning and Memory, 83, 125–133.PubMedCentralPubMedCrossRefGoogle Scholar
  62. King, V. R., & Corwin, J. V. (1992). Comparison of hemi-inattention produced by unilateral ­lesions of the posterior parietal cortex or medial agranular prefrontal cortex in rats: Neglect, extinction, and the role of stimulus distance. Behavioural Brain Research, 54, 117–131.CrossRefGoogle Scholar
  63. Kohler, C. (1985). Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. Journal of Comparative Neurology, 236, 504–522.PubMedCrossRefGoogle Scholar
  64. Kolb, B., & Walkey, J. (1987). Behavioural and anatomical studies of the posterior parietal cortex in the rat. Behavioural Brain Research, 23, 127–145.PubMedCrossRefGoogle Scholar
  65. Lee, I., & Kesner, R. P. (2003). Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. Journal of Neuroscience, 23, 1517–1523.PubMedGoogle Scholar
  66. Levy, W. B. (1996). A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus, 6, 579–590.PubMedCrossRefGoogle Scholar
  67. Lipton, P, A., Alvarez, P., & Eichenbaum, H. (1999). Crossmodal associative memory representation in rodent orbitofrontal cortex. Neuron, 22, 349–359.PubMedCrossRefGoogle Scholar
  68. Long, J. M., & Kesner, R. P. (1998). The effects of hippocampal and parietal cortex lesions on memory for egocentric distance and spatial location information in rats. Behavioral Neuroscience, 112, 480–495.PubMedCrossRefGoogle Scholar
  69. Long, J. M., Mellem, J. E., & Kesner, R. P. (1998). The effects of parietal cortex lesions on an object/spatial location paired-associate task in rats. Psychobiology, 26, 128–133.Google Scholar
  70. Maaswinkel, H., Gispen, W. H., & Spruijut, B. M. (1996). Effects of an electrolytic lesion of the prelimbic area on anxiety-related and cognitive tasks in the rat. Behavioural Brain Research, 79, 51–59.PubMedCrossRefGoogle Scholar
  71. Marr, D. (1971). Simple memory: A theory for archicortex. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 262, 23–81.PubMedCrossRefGoogle Scholar
  72. McAlonan, K., & Brown, V. J. (2003). Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behavioural Brain Research, 146, 97–103.PubMedCrossRefGoogle Scholar
  73. McNaughton, B. L., & Morris, R. G. M. (1987). Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends in Neuroscience, 10, 408–415.CrossRefGoogle Scholar
  74. Muir, J. L., Everitt, B. J., & Robbins, T. W. (1996). The cerebral cortex of the rat and visual ­attentional function: Dissociable effects of mediofrontal, cingulate, anterior dorsolateral, and parietal cortex lesions on a five-choice serial reaction time ask. Cerebral Cortex, 6, 470–481.PubMedCrossRefGoogle Scholar
  75. Nadel, L. (1994). Multiple memory systems: What and why, an update. In D. L. Schacter & E. Tulving (Eds.), Memory systems 1994 (pp. 39–63). Cambridge: MIT Press.Google Scholar
  76. Neave, N., Lloyd, S., Sahgal, A., & Aggleton, J. P. (1994). Lack of effect of lesions in the ­anterior cingulate cortex and retrosplenial cortex on certain tests of spatial memory in the rat. ­Behavioural Brain Research, 65, 89–101.PubMedCrossRefGoogle Scholar
  77. Neill, W. T., & Mathis, K. M. (1995). Transfer-inappropriate processing: Negative priming and related phenomena. Psychological Learning and Motivation, 38, 1–44.CrossRefGoogle Scholar
  78. OʼKeefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Clarendon.Google Scholar
  79. Olton, D. S. (1983). Memory functions and the hippocampus. In W. Seifert (Ed.), Neurobiology of the hippocampus. New York: Academic.Google Scholar
  80. O’Reilly, R. C., & McClelland, J. L. (1994). Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade-off. Hippocampus, 4, 661–682.CrossRefGoogle Scholar
  81. Otto, T., & Eichenbaum, H. (1992). Complementary roles of the orbital prefrontal cortex and the perirhinal-entorhinal cortices in an odor-guided delayed-nonmatching-to-sample task. Behavioral Neuroscience, 106, 762–775.PubMedCrossRefGoogle Scholar
  82. Passingham, R. E., Myers, C., Rawlins, N., Lightfoot, V., Fearn, S., et al. (1988). Premotor cortex in the rat. Behavioral Neuroscience, 102, 101–109.Google Scholar
  83. Poucet, B. (1989). Object exploration, habituation, and response to a spatial change in rats ­following septal or medial frontal cortical damage. Behavioral Neuroscience, 103, 1009–1016.PubMedCrossRefGoogle Scholar
  84. Ragozzino, M. E., & Kesner, R. P. (1998). The effects of muscarinic cholinergic receptor blockade in the rat anterior cingulate and prelimbic/infralimbic cortices on spatial working memory. Neurobiology of Learning and Memory, 69, 241–257.PubMedCrossRefGoogle Scholar
  85. Ragozzino, M. E., & Kesner, R. P. (1999). The role of the agranular insular cortex in working memory for food reward value and allocentric space in rats. Behavioural Brain Research, 1, 103–112.Google Scholar
  86. Ragozzino, M. E., Adams, S., & Kesner, R. P. (1998). Differential involvement of the dorsal anterior cingulate and prelimbic-infralimbic areas of the rodent prefrontal cortex in spatial working memory. Behavioral Neuroscience, 112, 293–303.PubMedCrossRefGoogle Scholar
  87. Ragozzino, M. E., Wilcox, C., Raso, M., & Kesner, R. P. (1999a). Involvement of the medial prefrontal cortex subregions in strategy switching. Behavioral Neuroscience, 113, 32–41.PubMedCrossRefGoogle Scholar
  88. Ragozzino, M. E., Detrick, S., & Kesner, R. P. (1999b). Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. Journal of Neuroscience, 19, 4585–4594.PubMedGoogle Scholar
  89. Reep, R. L., Chandler, H. C., King, V., & Corwin, J. V. (1994). Rat posterior parietal cortex: Topography of cortico-cortical and thalamic connections. Experimental Brain Research, 100, 67–84.PubMedCrossRefGoogle Scholar
  90. Rogers, J. L., & Kesner, R. P. (2007). Hippocampal-parietal cortex interactions: Evidence from a disconnection study in the rat. Behavioural Brain Research, 179, 19–27.PubMedCentralPubMedCrossRefGoogle Scholar
  91. Rolls, E. T. (1996). A theory of hippocampal function in memory. Hippocampus, 6, 601–620.PubMedCrossRefGoogle Scholar
  92. Rolls, E. T., & Kesner, R. P. (2006). A computational theory of hippocampal function, and empirical tests of the theory. Progress in Neurobiology, 79, 1–48.PubMedCrossRefGoogle Scholar
  93. Rolls, E. T., & Treves, A. (1998). Neural networks and brain function. Oxford: Oxford University Press.Google Scholar
  94. Save, E., & Moghaddam, M. (1996). Effects of lesions of the associative parietal cortex on the acquisition and use of spatial memory in egocentric and allocentric navigation tasks in the rat. Behavioral Neuroscience, 110, 74–85.PubMedCrossRefGoogle Scholar
  95. Save, E., & Poucet, B. (2000). Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation. Behavioural Brain Research, 109, 195–206.PubMedCrossRefGoogle Scholar
  96. Save, E., Buhot, M.-C., Foreman, N., & Thinus-Blanc, C. (1992). Exploratory activity and ­response to a spatial change in rats with hippocampal or posterior parietal cortical lesions. Behavioural Brain Research, 47, 113–127.PubMedCrossRefGoogle Scholar
  97. Schacter, D. L. (1987). Implicit memory: History and current status. Journal of Experimental Psychology: Learning, Memory, and Cognition, 13, 501–518.Google Scholar
  98. Schacter, D. L., & Tulving, E. (Eds.). (1994). Memory systems 1994. Cambridge: MIT Press.Google Scholar
  99. Schoenbaum, G., Chiba, A. A., & Gallagher, M. (1999). Neural encoding in orbitofrotal cortex and basolateral amygdala during olfactory discrimination learning. Journal of Neuroscience, 19, 1876–1884.PubMedGoogle Scholar
  100. Seamans, J. K., Floresco, S. B., & Phillips, A. G. (1995). Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behavioural Neuroscience, 109, 1063–1073.CrossRefGoogle Scholar
  101. Shapiro, M. L., & Olton, D. S. (1994). Hippocampal function and interference. In D. L. Schacter & E. Tulving (Eds.), Memory systems 1994 (pp. 141–146). Cambridge: MIT Press.Google Scholar
  102. Shaw, C., & Aggleton, J. P. (1993). The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats. Behavioural Brain Research, 54, 91–102.PubMedCrossRefGoogle Scholar
  103. Spear, N. F. (1976). Retrieval of memories: A psychobiological approach. In W. K. Estes (Ed.), Handbook of learning and cognitive processes (Vol. 4). Attention and memory. Hillsdale: Erlbaum.Google Scholar
  104. Squire, L. R. (1994). Declarative and nondeclarative memory: Multiple brain systems supporting learning and memory. In D. L. Schacter & E. Tulving (Eds.), Memory systems 1994 (pp. 203–231). Cambridge: MIT Press.Google Scholar
  105. Squire, L. R., Stark, C. E., & Clark, R. E. (2004). The medial temporal lobe. Annual Review Neuroscience, 27, 279–306.CrossRefGoogle Scholar
  106. Tees, R. C. (1999). The effects of posterior parietal cortex and posterior temporal cortical lesions on multimodal spatial and nonspatial competencies in rats. Behavioural Brain Research, 106, 55–73.PubMedCrossRefGoogle Scholar
  107. Tulving, E. (1983). Elements of episodic memory. Oxford: Clarendon.Google Scholar
  108. Underwood, B. J. (1969). Attributes of memory. Psychology Review, 76, 559–573.CrossRefGoogle Scholar
  109. Uylings, H. B. M., & van Eden, C. G. (1990). Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Progress in Brain Research, 85, 31–61.PubMedCrossRefGoogle Scholar
  110. Van Groen, T., & Wyss, J. M. (1990). The connections of presubiculum and parasubiculum in the rat. Brain Research, 518, 227–243.PubMedCrossRefGoogle Scholar
  111. Vertes, R. P. (2006). Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience, 142, 1–20.PubMedCrossRefGoogle Scholar
  112. Weeden, C. S. S., Hu, N. J., Ho, L. U. N., & Kesner, R. P. (2014). The role of the ventral dentate gyrus in olfactory pattern separation. Hippocampus, 24, 553–559.PubMedCrossRefGoogle Scholar
  113. Whishaw, I. Q., Tomie, J., & Kolb, B. (1992). Ventrolateral prefrontal cortex lesions in rats impair the acquisition and retention of a tactile-olfactory configural task. Behavioral Neuroscience, 106, 597–603.PubMedCrossRefGoogle Scholar
  114. Winocur, G. (1991). Functional dissociation of the hippocampus and prefrontal cortex in learning and memory. Psychobiology, 19, 11–20.Google Scholar
  115. Winocur, G., & Eskes, G. (1998). Prefrontal cortex and caudate nucleus in conditional associative learning: Dissociated effects of selective brain lesions in rats. Behavioral Neuroscience, 112, 89–101.PubMedCrossRefGoogle Scholar
  116. Wise, S. P., Murray, E. A., & Gerfen, C. R. (1996). The frontal cortex-basal ganglia system in primates. Critical Reviews in Neurobiology, 10, 317–356.PubMedCrossRefGoogle Scholar
  117. Witter, M. P., Groenewegen, H. J., Lopes da Silva, F. H., & Lohman, A. H. (1989). Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Progress in Neurobiology, 33, 161–253.PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of PsychologyUniversity of UtahSalt Lake CityUSA

Personalised recommendations