Skip to main content
SpringerLink
Log in

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

  • Chapter
  • First Online:
The Neurobiological Basis of Memory

  • 1428 Accesses

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Cohen, N. J., & Eichenbaum, H. B. (1993). Memory, amnesia, and hippocampal function. ­Cambridge: MIT Press.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Day, M., Langston, R., & Morris, R. G. (2003). Glutamate-receptor-mediated encoding and ­retrieval of paired-associate learning. Nature, 424, 205–209.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Delatour, B., & Gisquet-Verrier, P. (1996). Prelimbic cortex specific lesions disrupt delayed ­variable response tasks in the rat. Behavioral Neuroscience, 110, 1282–1298.

    Article  PubMed  Google Scholar 

  • DiMattia, B. V., & Kesner, R. P. (1988). Spatial cognitive maps: Differential role of parietal cortex and hippocampal formation. Behavioral Neuroscience, 102, 471–480.

    Article  PubMed  Google Scholar 

  • 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 

  • Eichenbaum, H. (2004). Hippocampus: Cognitive processes and neural representation that ­underlie declarative memory. Neuron, 44, 109–120.

    Article  PubMed  Google Scholar 

  • Eichenbaum, H., Clegg, R. A., & Feeley, A. (1983). Reexamination of functional subdivisions of the rodent prefrontal cortex. Experimental Neurology, 79, 434–451.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Gilbert, P. E., Kesner, R. P., & Lee, I. (2001). Dissociating hippocampal subregions: A double ­dissociation between dentate gyrus and CA1. Hippocampus, 11, 626–636.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Kesner, R. P. (1989). Retrospective and prospective coding of information: Role of the medial prefrontal cortex. Experimental Brain Research, 74, 163–167.

    Article  PubMed  Google Scholar 

  • Kesner, R. P. (1990). Memory for frequency in rats: Role of the hippocampus and medial prefrontal cortex. Behavioral and Neural Biology, 53, 402–410.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • Kesner, R. P. (1999). Perirhinal cortex and hippocampus mediate parallel processing of object and spatial location information. Behavioural and Brain Sciences, 22, 455–479.

    Article  Google Scholar 

  • Kesner, R. P. (2000a). Subregional analysis of mnemonic functions of the prefrontal cortex in the rat. Psychobiology, 28, 219–228.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Kesner, R. P., & Holbrook, T. (1987). Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia, 25, 653–664.

    Article  PubMed  Google Scholar 

  • Kesner, R. P., & Hopkins, R. O. (2006). Mnemonic functions of the hippocampus: A comparison between animals and humans. Biological Psychology, 73, 3–18.

    Article  PubMed  Google Scholar 

  • Kesner, R. P., & Warthen, D. K. (2010). Implications of CA3 NMDA and opiate receptors for spatial pattern completion in rats. Hippocampus, 20, 550–557.

    PubMed  Google Scholar 

  • Kesner, R. P., DiMattia, B. V., & Crutcher, K. A. (1987). Evidence for neocortical involvement in reference memory. Behavioral and Neural Biology, 47, 40–53.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Kesner, R. P., Fansworth, G., & Kametani, H. (1991). Role of parietal cortex and hippocampus in representing spatial information. Cerebral Cortex, 1, 367–373.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Kohler, C. (1985). Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. Journal of Comparative Neurology, 236, 504–522.

    Article  PubMed  Google Scholar 

  • Kolb, B., & Walkey, J. (1987). Behavioural and anatomical studies of the posterior parietal cortex in the rat. Behavioural Brain Research, 23, 127–145.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Lipton, P, A., Alvarez, P., & Eichenbaum, H. (1999). Crossmodal associative memory representation in rodent orbitofrontal cortex. Neuron, 22, 349–359.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • Marr, D. (1971). Simple memory: A theory for archicortex. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 262, 23–81.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • Neill, W. T., & Mathis, K. M. (1995). Transfer-inappropriate processing: Negative priming and related phenomena. Psychological Learning and Motivation, 38, 1–44.

    Article  Google Scholar 

  • OʼKeefe, J., & Nadel, L. (1978). The hippocampus as a cognitive map. Oxford: Clarendon.

    Google Scholar 

  • Olton, D. S. (1983). Memory functions and the hippocampus. In W. Seifert (Ed.), Neurobiology of the hippocampus. New York: Academic.

    Google Scholar 

  • O’Reilly, R. C., & McClelland, J. L. (1994). Hippocampal conjunctive encoding, storage, and recall: Avoiding a trade-off. Hippocampus, 4, 661–682.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed Central  PubMed  Google Scholar 

  • Rolls, E. T. (1996). A theory of hippocampal function in memory. Hippocampus, 6, 601–620.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Rolls, E. T., & Treves, A. (1998). Neural networks and brain function. Oxford: Oxford University Press.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Schacter, D. L. (1987). Implicit memory: History and current status. Journal of Experimental Psychology: Learning, Memory, and Cognition, 13, 501–518.

    Google Scholar 

  • Schacter, D. L., & Tulving, E. (Eds.). (1994). Memory systems 1994. Cambridge: MIT Press.

    Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  Google Scholar 

  • 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 

  • 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 

  • Squire, L. R., Stark, C. E., & Clark, R. E. (2004). The medial temporal lobe. Annual Review Neuroscience, 27, 279–306.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Tulving, E. (1983). Elements of episodic memory. Oxford: Clarendon.

    Google Scholar 

  • Underwood, B. J. (1969). Attributes of memory. Psychology Review, 76, 559–573.

    Article  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Van Groen, T., & Wyss, J. M. (1990). The connections of presubiculum and parasubiculum in the rat. Brain Research, 518, 227–243.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Winocur, G. (1991). Functional dissociation of the hippocampus and prefrontal cortex in learning and memory. Psychobiology, 19, 11–20.

    Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychology, University of Utah, 380 S 1530 E, Rm 502, 84112, Salt Lake City, UT, USA

    Raymond P. Kesner PhD

Authors
  1. Raymond P. Kesner PhD
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Raymond P. Kesner PhD .

Editor information

Editors and Affiliations

  1. Department of Psychology, Radford University, Radford, Virginia, USA

    Pamela A. Jackson

  2. Department of Cognitive Science, University of California-San Diego, La Jolla, California, USA

    Andrea A. Chiba

  3. Department of Neurological Surgery and Center for Neuroscience, University of California-Davis, Davis, California, USA

    Robert F. Berman

  4. Department of Psychology, University of Illinois at Chicago, Chicago, Illinois, USA

    Michael E. Ragozzino

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Kesner, R. (2016). Exploration of the Neurobiological Basis for a Three-System, Multi-attribute Model of Memory. In: Jackson, P., Chiba, A., Berman, R., Ragozzino, M. (eds) The Neurobiological Basis of Memory. Springer, Cham. https://doi.org/10.1007/978-3-319-15759-7_1

Download citation

Publish with us

Policies and ethics

Search

Navigation