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. There have been a number of attempts to divide learning and memory into multiple memory systems. Schacter and Tulving, Memory systems 1994. MIT Press, Cambridge (1994) have suggested that one needs to define memory systems in terms of the kind of information to be represented, the processes associated with the operation of each system, and the neurobiological substrates, including neural structures and mechanisms, that subserve each system. Furthermore, it is likely that within each system there are multiple forms or subsystems associated with each memory system and there are likely to be multiple processes that define the operation of each system. Finally, there are probably multiple neural structures that form the overall substrate of a memory system.
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References
Bussey TJ, Muir JL, Everitt BJ, Robbins TW (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. Behav Brain Res 82:45–56
Bussey TJ, Muir JL, Everitt BJ, Robbins TW (1997) Triple dissociation of anterior cingulate, posterior cingulate, and medial frontal cortices on visual discrimination tasks using a touchscreen testing procedure for the rat. Behav Neurosci 111:920–936
Chiba AA, Kesner RP, Reynolds AM (1994) Memory for spatial location as a function of temporal lag in rats: role of hippocampus and medial prefrontal cortex. Behav Neural Biol 61:123–131
Chiba AA, Kesner RP, Gibson CJ (1997) Memory for temporal order of new and familiar spatial location sequences: Role of the medial prefrontal cortex. Learning and Memory 4:311–317
Chiba AA, Kesner RP, Jackson P (2002) Two forms of spatial memory: a double dissociation between the parietal cortex and the hippocampus in the rat. Behav Neurosci 116:874–883
Cho YH, Kesner RP (1996) Involvement of entorhinal cortex or parietal cortex in long-term spatial discrimination memory in rats: retrograde amnesia. Behav Neurosci 110:436–442
Cho YH, Kesner RP, Brodale S (1995) Retrograde and anterograde amnesia for spatial discrimination in rats: role of hippocampus, entorhinal cortex and parietal cortex. Psychobiology 23:185–194
Churchwell JC, Kesner RP (2011) Hippocampal-prefrontal dynamics in spatial working memory: interactions and independent parallel processing. Behav Brain Res 225:389–395
Cohen NJ, Eichenbaum HB (1993) Memory, amnesia, and hippocampal function. MIT Press, Cambridge
Corwin JV, Fussinger M, Meyer RC, King VR, Reep RL (1994) Bilateral destruction of the ventrolateral orbital cortex produces allocentric but not egocentric spatial deficits in rats. Behav Brain Res 61:79–86
Day M, Langston R, Morris RG (2003) Glutamate-receptor-mediated encoding and retrieval of paired-associate learning. Nature 424:205–209
deBruin JPC, Swinkels WAM, deBrabander JM (1997) Response learning of rats in a Morris water maze: Involvement of the medial prefrontal cortex. Behav Brain Res 85:47–55
DeCoteau WE, Kesner RP (1998) Effects of hippocampal and parietal cortex lesions on the processing of multiple object scenes. Behav Neurosci 112:68–82
DeCoteau WE, Kesner RP, Williams JM (1997) Short-term memory for food reward magnitude: the role of the prefrontal cortex. Behav Brain Res 88:239–249
Delatour B, Gisquet-Verrier P (1996) Prelimbic cortex specific lesions disrupt delayed variable response tasks in the rat. Behav Neurosci 110:1282–1298
DiMattia BV, Kesner RP (1988) Spatial cognitive maps: Differential role of parietal cortex and hippocampal formation. Behav Neurosci 102:471–480
Eichenbaum H (1994) The hippocampal system and declarative memory in humans and animals: experimental analysis and historical origins. In Schacter DL, Tulving E (eds) Memory systems 1994. MIT Press, Cambridge, pp 39–63
Eichenbaum H (2004) Hippocampus: cognitive processes and neural representation that underlie declarative memory. Neuron 44:109–120
Eichenbaum H, Clegg RA, Feeley A (1983) Reexamination of functional subdivisions of the rodent prefrontal cortex. Exp Neurol 79:434–451
Ennaceur A, Neave N, Aggleton JP (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. Exp Brain Res 113:509–519
Estes WK (1986) Memory for temporal information. In: Michon JA, Jackson JL (eds) Time, mind and behavior. Springer, New York, pp 151–168
Ferbinteanu J, Holsinger RM, McDonald RJ (1999) Lesions of the medial or lateral perforant path have different effects on hippocampal contributions to place learning and fear conditioning to context. Behav Brain Res 101:65–84
Foreman N, Save E, Thinus-Blanc C, Buhot MC (1992) Visually guided locomotion, distractibility, and the missing-stimulus effect in hooded rates with unilateral or bilateral lesions of parietal cortex. Behav Neurosci 106:529–538
Gilbert PE, Kesner RP (2002a) The amygdala but not the hippocampus is involved in pattern separation based on reward value. Neurobiol Learn Mem 77:338–353
Gilbert PE, Kesner RP (2002b) Role of the rodent hippocampus in paired-associate learning involving associations between a stimulus and a spatial location. Behav Neurosci 116:63–71
Gilbert PE, Kesner RP (2003a) Recognition memory for complex visual discrimination is influenced by stimulus interference in rodents with perirhinal cortex damage. Learn Mem 10:525–530
Gilbert PE, Kesner RP (2003b) Localization of function within the dorsal hippocampus: the role of the CA3 subregion in paired-associate learning. Behav Neurosci 117:1385–1394
Gilbert PE, Kesner RP (2006) The role of dorsal CA3 hippocampal subregion in spatial working memory and pattern separation. Behav Brain Res 169:142–149
Gilbert PE, Kesner RP, Lee I (2001) Dissociating hippocampal subregions: a double dissociation between dentate gyrus and CA1. Hippocampus 11:626–636
Gold E, Kesner RP (2005) The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 15:808–814
Hafting T, Fyhn M, Molden S, Moser MB, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806
Hargreaves EL, Rao G, Lee I, Knierim JJ (2005) Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 308:1792–1794
Harrison LD, Mair RG (1996) A comparison of the effects of frontal cortical and thalamic lesions on measures of spatial learning and memory in the rat. Behav Brain Res 75:195–206
Hasselmo ME, Wyble BP (1997) Free recall and recognition in a network model of the hippocampus: simulating effects of scopolamine on human memory function. Behav Brain Res 89:1–34
Ho JW-T, Narduzzo KE, Outram A, Tinsley CJ, Henley JM, Warburton EC, Brown MW (2011) Contributions of area Te2 to rat recognition memory. Learn Mem 18:493–501
Hunsaker MR, Mooy GG, Swift JS, Kesner RP (2007) Dissociations of the medial and lateral perforant path projections into dorsal DG, CA3, and CA1 for spatial and nonspatial (visual object) information processing. Behav Neurosci 121:742–750
Hunsaker MR, Lee B, Kesner RP (2008) Evaluating the temporal context of episodic memory: the role of CA3 and CA1. Behav Brain Res 188:310–315
Jackson PA, Kesner RP, Amann K (1998) Memory for duration: role of hippocampus and medial prefrontal cortex. Neurobiol Learn Mem 70:328–348
Jay TM, Witter MP (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. J Comp Neurol 313:574–586
Kesner RP (1989) Retrospective and prospective coding of information: role of the medial prefrontal cortex. J Exper Brain Res 74:163–167
Kesner RP (1990) Memory for frequency in rats: role of the hippocampus and medial prefrontal cortex. Behav Neural Biol 53:402–410
Kesner RP (1998a) Neural mediation of memory for time: role of the hippocampus and medial prefrontal cortex. Psychon Bull Rev 5:585–596
Kesner RP (1998b) Neurobiological views of memory. In: Martinez JL, Kesner RP (eds) The neurobiology of learning and memory. Academic, San Diego, pp 361–416
Kesner RP (1999) Perirhinal cortex and hippocampus mediate parallel processing of object and spatial location information. Behav Brain Sci 22:455–479
Kesner RP (2000a) Subregional analysis of mnemonic functions of the prefrontal cortex in the rat. Psychobiology 28:219–228
Kesner RP (2000b) Behavioral analysis of the contribution of the hippocampus and parietal cortex to the processing of information: Interactions and dissociations. Hippocampus 10:483–490
Kesner RP (2007) Neurobiological views of memory. In: Kesner RP, Martinez JL (eds) The neurobiology of learning and memory, 2nd edn. Academic Press, San Diego, CA, pp 271–304
Kesner RP, Churchwell JC (2011) An analysis of rat prefrontal cortex in mediating executive function. Neurobiol Learn Mem 96:417–431
Kesner RP, Creem-Regehr SH (2013) Parietal contributions to spatial cognition. In: Nadel L, Waller D (eds) Handbook of spatial cognition. American Psychological Association, Washington, pp 35–64
Kesner RP, Gilbert P (2006) The role of the medial caudate nucleus, but not the hippocampus, in a matching-to sample task for a motor response. Eur J Neurosci 23:1888–1894
Kesner RP, Holbrook T (1987) Dissociation of item and order spatial memory in rats following medial prefrontal cortex lesions. Neuropsychologia 25:653–664
Kesner RP, Hopkins RO (2006) Mnemonic functions of the hippocampus: a comparison between animals and humans. Biol Psychol 73:3–18
Kesner RP, Warthen DK (2010) Implications of CA3 NMDA and opiate receptors for spatial pattern completion in rats. Hippocampus 20:550–557
Kesner RP, DiMattia BV, Crutcher KA (1987) Evidence for neocortical involvement in reference memory. Behav Neural Biol 47:40–53
Kesner RP, Farnsworth G, DiMattia BV (1989) Double-dissociation of egocentric and allocentric space following medial prefrontal and parietal cortex lesions in the rat. Behav Neurosci 103:956–961
Kesner RP, Fansworth G, Kametani H (1991) Role of parietal cortex and hippocampus in representing spatial information. Cereb Cortex 1:367–373
Kesner RP, Bolland B, Dakis M (1993) Memory for spatial locations, motor responses, and objects: triple dissociations among the hippocampus, caudate nucleus and extrastriate visual cortex. Exp Brain Res 93:462–470
Kesner RP, Hunt ME, Williams JM, Long JM (1996) Prefrontal cortex and working memory for spatial response, spatial location, and visual object information in the rat. Cereb Cortex 6:311–318
Kesner RP, Lee I, Gilbert P (2004) A behavioral assessment of hippocampal function based on a subregional analysis. Reviews Neuroscience 15:333–351
Kesner RP, Hunsaker MR, Warthen MW (2008) The CA3 subregion of the hippocampus is critical for episodic memory processing by means of relational encoding in rats. Behav Neurosci 122:1217–1225
Kim J, Ragozzino ME (2005) The involvement of the orbitofrontal cortex in learning under changing task contingencies. Neurobiol Learn Mem 83:125–133
King VR, Corwin JV (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. Behav Brain Res 54:117–131
Kohler C (1985) Intrinsic projections of the retrohippocampal region in the rat brain. I. The subicular complex. J Comp Neurol 236:504–522
Kolb B, Walkey J (1987) Behavioural and anatomical studies of the posterior parietal cortex in the rat. Behav Brain Res 23:127–145
Lee I, Kesner RP (2003) Time-dependent relationship between the dorsal hippocampus and the prefrontal cortex in spatial memory. J Neurosci 23:1517–1523
Levy WB (1996) A sequence predicting CA3 is a flexible associator that learns and uses context to solve hippocampal-like tasks. Hippocampus 6:579–590
Lipton PA, Alvarez P, Eichenbaum H (1999) Crossmodal associative memory representation in rodent orbitofrontal cortex. Neuron 22:349–359
Long JM, Kesner RP (1998) The effects of hippocampal and parietal cortex lesions on memory for egocentric distance and spatial location information in rats. Behav Neurosci 112:480–495
Long JM, Mellem JE, Kesner RP (1998) The effects of parietal cortex lesions on an object/spatial location paired-associate task in rats. Psychobiology 26:128–133
Maaswinkel H, Gispen WH, Spruijut BM (1996) Effects of an electrolytic lesion of the prelimbic area on anxiety-related and cognitive tasks in the rat. Behav Brain Res 79:51–59
Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc B: Biol Sci 262:23–81
McAlonan K, Brown VJ (2003) Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav Brain Res 146:97–103
McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415
Muir JL, Everitt BJ, Robbins TW (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. Cereb Cortex 6:470–481
Nadel L (1994) Multiple memory systems: what and why, an update. In Schacter DL, Tulving E (eds) Memory systems 1994. MIT Press, Cambridge, pp 39–63
Neave N, Lloyd S, Sahgal A, Aggleton JP (1994) Lack of effect of lesions in the anterior cingulate cortex and retrosplenial cortex on certain tests of spatial memory in the rat. Behav Brain Res 65:89–101
Neill WT, Mathis KM (1995) Transfer-inappropriate processing: negative priming and related phenomena. Psychol Learn Motiv 38:1–44
O’Reilly RC, McClelland JL (1994) Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus 4:661–682
O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Clarendon Press, Oxford
Olton DS (1983) Memory functions and the hippocampus. In: Seifert W (ed) Neurobiology of the hippocampus. Academic, New York
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. Behav Neurosci 106:762–775
Passingham RE, Myers C, Rawlins N, Lightfoot V, Fearn S et al (1988) Premotor cortex in the rat. Behav Neurosci 102:101–109
Poucet B (1989) Object exploration, habituation, and response to a spatial change in rats following septal or medial frontal cortical damage. Behav Neurosci 103:1009–1016
Ragozzino ME, Kesner RP (1998) The effects of muscarinic cholinergic receptor blockade in the rat anterior cingulate and prelimbic/infralimbic cortices on spatial working memory. Neurobiol Learn Mem 69:241–257
Ragozzino ME, Kesner RP (1999) The role of the agranular insular cortex in working memory for food reward value and allocentric space in rats. Behav Brain Res 1:103–112
Ragozzino ME, Adams S, Kesner RP (1998) Differential involvement of the dorsal anterior cingulate and prelimbic-infralimbic areas of the rodent prefrontal cortex in spatial working memory. Behav Neurosci 112:293–303
Ragozzino ME, Wilcox C, Raso M, Kesner RP (1999a) Involvement of the medial prefrontal cortex subregions in strategy switching. Behav Neurosci 113:32–41
Ragozzino ME, Detrick S, Kesner RP (1999b) Involvement of the prelimbic-infralimbic areas of the rodent prefrontal cortex in behavioral flexibility for place and response learning. J Neurosci 19:4585–4594
Reep RL, Chandler HC, King V, Corwin JV (1994) Rat posterior parietal cortex: topography of cortico-cortical and thalamic connections. Exp Brain Res 100:67–84
Rogers JL, Kesner RP (2007) Hippocampal-parietal cortex interactions: evidence from a disconnection study in the rat. Behav Brain Res 179:19–27
Rolls ET (1996) A theory of hippocampal function in memory. Hippocampus 6:601–620
Rolls ET, Kesner RP (2006) A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 79:1–48
Rolls ET, Treves A (1998) Neural networks and brain function. Oxford University Press, Oxford
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. Behav Neurosci 110:74–85
Save E, Poucet B (2000) Involvement of the hippocampus and associative parietal cortex in the use of proximal and distal landmarks for navigation. Behav Brain Res 109:195–206
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. Behav Brain Res 47:113–127
Schacter DL (1987) Implicit memory: history and current status. J Exp Psychol Learn Mem Cogn 13:501–518
Schacter DL, Tulving E (eds) (1994) Memory systems 1994. MIT Press, Cambridge
Schoenbaum G, Chiba AA, Gallagher M (1999) Neural encoding in orbitofrotal cortex and basolateral amygdala during olfactory discrimination learning. J Neurosci 19:1876–1884
Seamans JK, Floresco SB, Phillips AG (1995) Functional differences between the prelimbic and anterior cingulate regions of the rat prefrontal cortex. Behav Neurosci 109:1063–1073
Shapiro ML, Olton DS (1994) Hippocampal function and interference. In: Schacter DL, Tulving E (eds) Memory systems 1994. MIT Press, Cambridge, pp 141–146
Shaw C, Aggleton JP (1993) The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats. Behav Brain Res 54:91–102
Spear NF (1976) Retrieval of memories: a psychobiological approach In Estes WK (ed) Handbook of learning and cognitive processes (vol 4). Attention and memory. Erlbaum, Hillsdale
Squire LR (1994) Declarative and nondeclarative memory: multiple brain systems supporting learning and memory. In: Schacter DL, Tulving E (eds) Memory systems 1994. MIT Press, Cambridge, pp 203–231
Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306
Tees RC (1999) The effects of posterior parietal cortex and posterior temporal cortical lesions on multimodal spatial and nonspatial competencies in rats. Behav Brain Res 106:55–73
Tulving E (1983) Elements of episodic memory. Clarendon, Oxford
Underwood BJ (1969) Attributes of memory. Psychol Rev 76:559–573
Uylings HBM, van Eden CG (1990) Qualitative and quantitative comparison of the prefrontal cortex in rat and in primates, including humans. Prog Brain Res 85:31–61
Van Groen T, Wyss JM (1990) The connections of presubiculum and parasubiculum in the rat. Brain Res 518:227–243
Vertes RP (2006) Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142:1–20
Weeden CSS, Hu NJ, Ho LUN, Kesner RP (2014) The role of the ventral dentate gyrus in olfactory pattern separation. Hippocampus 24:553–559
Whishaw IQ, Tomie J, Kolb B (1992) Ventrolateral prefrontal cortex lesions in rats impair the acquisition and retention of a tactile-olfactory configural task. Behav Neurosci 106:597–603
Winocur G (1991) Functional dissociation of the hippocampus and prefrontal cortex in learning and memory. Psychobiology 19:11–20
Winocur G, Eskes G (1998) Prefrontal cortex and caudate nucleus in conditional associative learning: dissociated effects of selective brain lesions in rats. Behav Neurosci 112:89–101
Wise SP, Murray EA, Gerfen CR (1996) The frontal cortex-basal ganglia system in primates. Crit Rev Neurobiol 10:317–356
Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33:161–253
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Kesner, R.P. (2016). Exploration of the Neurobiological Basis for a Three-System, Multiattribute Model of Memory. In: Clark, R.E., Martin, S. (eds) Behavioral Neuroscience of Learning and Memory. Current Topics in Behavioral Neurosciences, vol 37. Springer, Cham. https://doi.org/10.1007/7854_2016_454
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