Attribute Memory Model and Behavioral Neurophysiology of Memory

  • Inah LeeEmail author
  • Choong-Hee Lee


Theories have been proposed to account for the multiple memory systems in the brain. Among those, the attribute theory for memory was originally proposed by Kesner. According to the theory, there are six major attributes for defining key aspects of an event. The event, once experienced, leaves its memory in the brain for short term and later becomes consolidated into a long-term memory. The attribute memory model proposes that the former type is processed by an event-based memory system and the latter type is handled by a knowledge-based memory system. The model also proposes a rule-based memory system (which is argued in this chapter as a subsystem of the knowledge-based memory system). The attribute memory model describes how different attributes recruit specific brain regions and how they interact. Computational information processes such as pattern separation and completion have also been proposed by the theory along with their associated subfields in the hippocampus. The model has always been tested in Kesner-style memory tasks, that is, goal-directed memory tasks using positive rewards. Such goal-directed tasks have provided great insights into how different memory systems and associated brain regions work in natural settings. Finding neurophysiological correlates of behavioral measures in these “freely moving” animals, however, poses a great technical challenge when one wants to record single-unit activity at the same time. As a means to continuing the Kesner-style behavioral probing in freely moving animals while analyzing single-unit activity rigorously, one needs some artful modifications in original behavioral paradigms to accommodate both behavioral and electrophysiological components. Once successfully implemented, such modifications would help physiologically test the attribute model of memory.


Attribute theory Behavioral electrophysiology Goal-directed task Object-place paired associate Spatial memory Event memory 


  1. Barnes, D. C., Hofacer, R. D., Zaman, A. R., Rennaker, R. L., & Wilson, D. A. (2008). Olfactory perceptual stability and discrimination. Nature Neuroscience, 11(12), 1378–1380. doi:10.1038/Nn.2217.PubMedCentralCrossRefPubMedGoogle Scholar
  2. Bartko, S. J., Vendrell, I., Saksida, L. M., & Bussey, T. J. (2011). A computer-automated touchscreen paired-associates learning (PAL) task for mice: Impairments following administration of scopolamine or dicyclomine and improvements following donepezil. Psychopharmacology (Berl), 214(2), 537–548. doi:10.1007/s00213-010-2050-1.CrossRefGoogle Scholar
  3. Baxter, M. G. (2009). Involvement of medial temporal lobe structures in memory and perception. Neuron, 61(5), 667–677. doi:10.1016/j.neuron.2009.02.007.CrossRefPubMedGoogle Scholar
  4. Bussey, T. J., & Saksida, L. M. (2005). Object memory and perception in the medial temporal lobe: An alternative approach. Current Opinion in Neurobiology, 15(6), 730–737. doi:10.1016/j.conb.2005.10.014.CrossRefPubMedGoogle Scholar
  5. Dombeck, D. A., Harvey, C. D., Tian, L., Looger, L. L., & Tank, D. W. (2010). Functional imaging of hippocampal place cells at cellular resolution during virtual navigation. Nature Neuroscience, 13(11), 1433–1440. doi:10.1038/Nn.2648.PubMedCentralCrossRefPubMedGoogle Scholar
  6. Eichenbaum, H., & Cohen, Neal J. (2001). From conditioning to conscious recollection: Memory systems of the brain. New York: Oxford University Press.Google Scholar
  7. Gilbert, P. E., & Kesner, R. P. (2006). The role of the dorsal CA3 hippocampal subregion in spatial working memory and pattern separation. Behavioural Brain Research, 169(1), 142–149. doi:10.1016/j.bbr.2006.01.002.CrossRefPubMedGoogle Scholar
  8. Gilbert, P. E., Kesner, R. P., & DeCoteau, W. E. (1998). Memory for spatial location: Role of the hippocampus in mediating spatial pattern separation. Journal of Neuroscience, 18(2), 804–810.PubMedGoogle Scholar
  9. Gluck, M. A., Meeter, M., & Myers, C. E. (2003). Computational models of the hippocampal region: Linking incremental learning and episodic memory. Trends in Cognitive Sciences, 7(6), 269–276.CrossRefPubMedGoogle Scholar
  10. Hargreaves, E. L., Rao, G., Lee, I., & Knierim, J. J. (2005). Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science, 308(5729), 1792–1794. doi:10.1126/science.1110449.CrossRefPubMedGoogle Scholar
  11. 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(1–2), 1–34. doi:10.1016/S0166-4328(97)00048-X.CrossRefPubMedGoogle Scholar
  12. Jo, Y. S., & Lee, I. (2010a). Disconnection of the hippocampal-perirhinal cortical circuits severely disrupts object-place paired associative memory. Journal of Neuroscience, 30(29), 9850–9858. doi:10.1523/JNEUROSCI.1580-10.2010.CrossRefPubMedGoogle Scholar
  13. Jo, Y. S., & Lee, I. (2010b). Perirhinal cortex is necessary for acquiring, but not for retrieving object-place paired association. Learning & Memory, 17(2), 97–103. doi:10.1101/Lm.1620410.CrossRefGoogle Scholar
  14. Kesner, R. P. (1980). An attribute analysis of memory—the role of the hippocampus. Physiological Psychology, 8(2), 189–197.CrossRefGoogle Scholar
  15. Kesner, R. P. (2009). Tapestry of memory. Behavioral Neuroscience, 123(1), 1–13. doi:10.1037/A0014004.CrossRefPubMedGoogle Scholar
  16. Kesner, R. P. (2013). A process analysis of the CA3 subregion of the hippocampus. Front Cell Neuroscience, 7, 78. doi:10.3389/fncel.2013.00078.CrossRefGoogle Scholar
  17. Kesner, R. P., & Hardy, J. D. (1983). Long-term-memory for contextual attributes—dissociation of amygdala and hippocampus. Behavioural Brain Research, 8(2), 139–149. doi:10.1016/0166-4328(83)90050-5.CrossRefPubMedGoogle Scholar
  18. Kesner, R. P., & Rogers, J. (2004). An analysis of independence and interactions of brain substrates that subserve multiple attributes, memory systems, and underlying processes. Neurobiology of Learning and Memory, 82(3), 199–215. doi 10.1016/j.nlm.2004.05.007.CrossRefPubMedGoogle Scholar
  19. Kesner, R. P., & Rolls, E. T. (2001). Role of long-term synaptic modification in short-term memory. Hippocampus, 11(3), 240–250. doi:10.1002/Hipo.1040.CrossRefPubMedGoogle Scholar
  20. Kesner, R. P., & Williams, J. M. (1995). Memory for magnitude of reinforcement—dissociation between the amygdala and hippocampus. Neurobiology of Learning and Memory, 64(3), 237–244.CrossRefPubMedGoogle Scholar
  21. Kesner, R. P., Bolland, B. L., & Dakis, M. (1993). Memory for spatial locations, motor-responses, and objects—triple dissociation among the hippocampus, caudate-nucleus, and extrastriate visual-cortex. Experimental Brain Research, 93(3), 462–470.CrossRefPubMedGoogle Scholar
  22. Kesner, R. P., Gilbert, P. E., & Wallenstein, G. V. (2000). Testing neural network models of memory with behavioral experiments. Current Opinion in Neurobiology, 10(2), 260–265. doi:10.1016/S0959-4388(00)00067-2.CrossRefPubMedGoogle Scholar
  23. 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(6), 1217–1225. doi:10.1037/A0013592.CrossRefPubMedGoogle Scholar
  24. Kim, J. J., Delcasso, S., & Lee, I. (2011). Neural correlates of object-in-place learning in hippocampus and prefrontal cortex. Journal of Neuroscience, 31(47), 16991–17006. doi:10.1523/Jneurosci.2859-11.2011.PubMedCentralCrossRefPubMedGoogle Scholar
  25. Lee, I., & Kesner, R. P. (2002). Differential contribution of NMDA receptors in hippocampal subregions to spatial working memory. Nature Neuroscience, 5(2), 162–168. doi:10.1038/Nn790.CrossRefPubMedGoogle Scholar
  26. Lee, I., & Kesner, R. P. (2004). Encoding versus retrieval of spatial memory: Double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus, 14(1), 66–76. doi:10.1002/Hipo.10167.CrossRefPubMedGoogle Scholar
  27. Lee, I., & Solivan, F. (2010). Dentate gyrus is necessary for disambiguating similar object-place representations. Learning & Memory, 17(5), 252–258.CrossRefGoogle Scholar
  28. Lee, I., Yoganarasimha, D., Rao, G., & Knierim, J. J. (2004). Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature, 430(6998), 456–459. doi:10.1038/Nature02739.CrossRefPubMedGoogle Scholar
  29. Leutgeb, S., Leutgeb, J. K., Treves, A., Moser, M. B., & Moser, E. I. (2004). Distinct ensemble codes in hippocampal areas CA3 and CA1. Science, 305(5688), 1295–1298. doi:10.1126/science.1100265.CrossRefPubMedGoogle Scholar
  30. Leutgeb, J. K., Leutgeb, S., Moser, M. B., & Moser, E. I. (2007). Pattern separation in the dentate gyrus and CA3 of the hippocampus. Science, 315(5814), 961–966. doi:10.1126/science.1135801.CrossRefPubMedGoogle Scholar
  31. Marr, D. (1971). Simple memory—a theory for archicortex. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 262(841), 23–81. doi:10.1098/rstb.1971.0078.CrossRefGoogle Scholar
  32. McDonald, R.J., & White, N.M. (1993). A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behavioral Neuroscience, 107, 3–22.CrossRefPubMedGoogle Scholar
  33. Murray, E. A., Bussey, T. J., & Saksida, L. M. (2007). Visual perception and memory: A new view of medial temporal lobe function in primates and rodents. Annual Review of Neuroscience, 30, 99–122. doi:10.1146/annurev.neuro.29.051605.113046.CrossRefPubMedGoogle Scholar
  34. Niessing, J., & Friedrich, R. W. (2010). Olfactory pattern classification by discrete neuronal network states. Nature, 465(7294), 47–52. doi:10.1038/Nature08961.CrossRefPubMedGoogle Scholar
  35. Oreilly, R. C., & Mcclelland, J. L. (1994). Hippocampal conjunctive encoding, storage, and recall—avoiding a trade-off. Hippocampus, 4(6), 661–682. doi:10.1002/hipo.450040605.CrossRefGoogle Scholar
  36. Packard, M. G. (1999). Glutamate infused posttraining into the hippocampus or caudate-putamen differentially strengthens place and response learning. Proceedings of the National Academy of Sciences of the United States of America, 96(22), 12881–12886. doi:10.1073/pnas.96.22.12881.Google Scholar
  37. Packard, M. G., & McGaugh, J. L. (1996). Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiology of Learning and Memory, 65(1), 65–72. doi:10.1006/nlme.1996.0007.CrossRefPubMedGoogle Scholar
  38. Ravassard, P., Kees, A., Willers, B., Ho, D., Aharoni, D., Cushman, J., et al. (2013). Multisensory control of hippocampal spatiotemporal selectivity. Science, 340(6138), 1342–1346. doi:10.1126/science.1232655.PubMedCentralCrossRefPubMedGoogle Scholar
  39. Rolls, E. T. (1996). A theory of hippocampal function in memory. Hippocampus, 6(6), 601–620. doi:10.1002/(Sici)1098-1063(1996)6:63.0.Co;2–J.CrossRefPubMedGoogle Scholar
  40. Rolls, E. T., & Kesner, R. P. (2006). A computational theory of hippocampal function, and empirical tests of the theory. Progress in Neurobiology, 79(1), 1–48. doi:10.1016/j.pneurobio.2006.04.005.CrossRefPubMedGoogle Scholar
  41. Squire, L. R. (2004). Memory systems of the brain: A brief history and current perspective. Neurobiology of Learning and Memory, 82(3), 171–177. doi:10.1016/j.nlm.2004.06.005.CrossRefPubMedGoogle Scholar
  42. Squire, L. R., & Zola-Morgan, S. (1991). The medial temporal lobe memory system. Science, 253(5026), 1380–1386.CrossRefPubMedGoogle Scholar
  43. Suzuki, W. A. (2009). Perception and the medial temporal lobe: Evaluating the current evidence. Neuron, 61(5), 657–666. doi:10.1016/j.neuron.2009.02.008.CrossRefPubMedGoogle Scholar
  44. Treves, A., & Rolls, E. T. (1994). Computational analysis of the role of the hippocampus in memory. Hippocampus, 4(3), 374–391. doi:10.1002/hipo.450040319.CrossRefPubMedGoogle Scholar
  45. Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., et al. (2007). Schemas and memory consolidation. Science, 316(5821), 76–82. doi:10.1126/science.1135935.CrossRefPubMedGoogle Scholar
  46. Tse, D., Takeuchi, T., Kakeyama, M., Kajii, Y., Okuno, H., Tohyama, C., et al. (2011). Schema-dependent gene activation and memory encoding in neocortex. Science, 333(6044), 891–895. doi:10.1126/science.1205274.CrossRefPubMedGoogle Scholar
  47. Tulving, E. (1972). Episodic and semantic memory. In E. D. Tulving & W. Donaldson (Ed.), Organization of memory (pp. 382–402). New York: Academic.Google Scholar
  48. Tulving, E. (1985). How many memory-systems are there. American Psychologist, 40(4), 385–398. doi:10.1037/0003-066x.40.4.385.CrossRefGoogle Scholar
  49. Wallenstein, G. V., Eichenbaum, H., & Hasselmo, M. E. (1998). The hippocampus as an associator of discontiguous events. Trends in Neurosciences, 21(8), 317–323. doi:10.1016/S0166-2236(97)01220-4.CrossRefPubMedGoogle Scholar
  50. Yassa, M. A., & Stark, C. E. (2011). Pattern separation in the hippocampus. Trends in Neurosciences, 34(10), 515–525. doi:10.1016/j.tins.2011.06.006.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Brain and Cognitive Sciences, Laboratory for Behavioral NeurophysiologySeoul National UniversitySeoulRepublic of Korea

Personalised recommendations