The human hippocampus receives distinct signals via the lateral entorhinal cortex, typically associated with object features, and the medial entorhinal cortex, associated with spatial or contextual information. The existence of these distinct types of information calls for some means by which they can be managed in an appropriate way, by integrating them or keeping them separate as required to improve recognition. We hypothesize that several anatomical features of the hippocampus, including differentiation in connectivity between the superior/inferior blades of DG and the distal/proximal regions of CA3 and CA1, work together to play this information managing role. We construct a set of neural network models with these features and compare their recognition performance when given noisy or partial versions of contexts and their associated objects. We found that the anterior and posterior regions of the hippocampus naturally require different ratios of object and context input for optimal performance, due to the greater number of objects versus contexts. Additionally, we found that having separate processing regions in DG significantly aided recognition in situations where object inputs were degraded. However, split processing in both DG and CA3 resulted in performance tradeoffs, though the actual hippocampus may have ways of mitigating such losses. 1. Introduction We make sense of the world by comparing our immediate sensations with memories of similar situations. A very basic type of situation is an encounter with objects in a context. For example, objects such as a salt shaker, a glass, and a sink are expected in a kitchen. Even if these objects are encountered in an office, they suggest a kitchen-like function to the area (e.g., it is a kitchenette—not a work cubicle). In other words, the objects evoke the context in which they have been experienced in the past, and the context evokes objects that have been experienced there. The hippocampus, which is essential for the storage and retrieval of memories, is likely to play a central role in this associational process. In rats, the hippocampus is oriented along a dorsal-ventral axis, while in primates this axis becomes an anterior-posterior axis. In both species, signals reach the hippocampus via the entorhinal cortex (EC layers II and III), which can be divided into lateral and medial portions (denoted LEC and MEC, resp.). Both the LEC and MEC can be further subdivided into caudolateral and rostromedial bands, with the caudolateral bands projecting mainly to the posterior half of the hippocampus and the
References
[1]
M. P. Witter, G. W. Van Hoesen, and D. G. Amaral, “Topographical organization of the entorhinal projection to the dentate gyrus of the monkey,” Journal of Neuroscience, vol. 9, no. 1, pp. 216–228, 1989.
[2]
J. K. Leutgeb, S. Leutgeb, M. B. Moser, and E. I. Moser, “Pattern separation in the dentate gyrus and CA3 of the hippocampus,” Science, vol. 315, no. 5814, pp. 961–966, 2007.
[3]
C. B. Alme, R. A. Buzzetti, D. F. Marrone et al., “Hippocampal granule cells opt for early retirement,” Hippocampus, vol. 20, no. 10, pp. 1109–1123, 2010.
[4]
W. Deng, M. Mayford, and F. H. Gage, “Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice,” ELife, vol. 2, Article ID e00312, 2013.
[5]
L. M. Rangel and H. Eichenbaum, “What's new is older,” ELife, vol. 2, Article ID e00605, 2013.
[6]
R. C. O'Reilly and J. W. Rudy, “Conjunctive representations in learning and memory: principles of cortical and hippocampal function,” Psychological Review, vol. 108, no. 2, pp. 311–345, 2001.
[7]
A. Treves and E. T. Rolls, “Computational analysis of the role of the hippocampus in memory,” Hippocampus, vol. 4, no. 3, pp. 374–391, 1994.
[8]
M. P. Witter, “Intrinsic and extrinsic wiring of CA3: indications for connectional heterogeneity,” Learning & Memory, vol. 14, no. 11, pp. 705–713, 2007.
[9]
S. Zola-Morgan, L. R. Squire, and D. G. Amaral, “Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus,” Journal of Neuroscience, vol. 6, no. 10, pp. 2950–2967, 1986.
[10]
M. R. Hunsaker, G. G. Mooy, J. S. Swift, and R. P. Kesner, “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, vol. 121, no. 4, pp. 742–750, 2007.
[11]
M. R. Hunsaker, P. M. Fieldsted, J. S. Rosenberg, and R. P. Kesner, “Dissociating the roles of dorsal and ventral CA1 for the temporal processing of spatial locations, visual objects, and odors,” Behavioral Neuroscience, vol. 122, no. 3, pp. 643–650, 2008.
[12]
R. D. Burwell, “The parahippocampal region: corticocortical connectivity,” Annals of the New York Academy of Sciences, vol. 911, pp. 25–42, 2000.
[13]
C. B. Cave and L. R. Squire, “Equivalent impairment of spatial and nonspatial memory following damage to the human hippocampus,” Hippocampus, vol. 1, no. 3, pp. 329–340, 1991.
[14]
E. L. Hargreaves, G. Rao, I. Lee, and J. J. Knierim, “Neuroscience: major dissociation between medial and lateral entorhinal input to dorsal hippocampus,” Science, vol. 308, no. 5729, pp. 1792–1794, 2005.
[15]
S. Dennis and M. S. Humphreys, “A context noise model of episodic word recognition,” Psychological Review, vol. 108, no. 2, pp. 452–478, 2001.
[16]
S. Gaskin, A. Gamliel, M. Tardif, E. Cole, and D. G. Mumby, “Incidental (unreinforced) and reinforced spatial learning in rats with ventral and dorsal lesions of the hippocampus,” Behavioural Brain Research, vol. 202, no. 1, pp. 64–70, 2009.
[17]
M. B. Moser and E. I. Moser, “Functional differentiation in the hippocampus,” Hippocampus, vol. 8, no. 6, pp. 608–619, 1998.
[18]
R. E. Clark, S. M. Zola, and L. R. Squire, “Impaired recognition memory rats after damage to the hippocampus,” Journal of Neuroscience, vol. 20, no. 23, pp. 8853–8860, 2000.
[19]
M. N. De Lima, T. Luft, R. Roesler, and N. Schr？der, “Temporary inactivation reveals an essential role of the dorsal hippocampus in consolidation of object recognition memory,” Neuroscience Letters, vol. 405, no. 1-2, pp. 142–146, 2006.
[20]
O. Hardt, P. V. Migues, M. Hastings, J. Wong, and K. Nader, “PKMζ maintains 1-day- and 6-day-old long-term object location but not object identity memory in dorsal hippocampus,” Hippocampus, vol. 20, no. 6, pp. 691–695, 2010.
[21]
D. G. Mumby, S. Gaskin, M. J. Glenn, T. E. Schramek, and H. Lehmann, “Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts,” Learning and Memory, vol. 9, no. 2, pp. 49–57, 2002.
[22]
J. A. Ainge, C. Heron-Maxwell, P. Theofilas, P. Wright, L. De Hoz, and E. R. Wood, “The role of the hippocampus in object recognition in rats: examination of the influence of task parameters and lesion size,” Behavioural Brain Research, vol. 167, no. 1, pp. 183–195, 2006.
[23]
J. R. Manns and H. Eichenbaum, “A cognitive map for object memory in the hippocampus,” Learning and Memory, vol. 16, no. 10, pp. 616–624, 2009.
[24]
R. S. Rosenbaum, S. K？hler, D. L. Schacter et al., “The case of K.C.: contributions of a memory-impaired person to memory theory,” Neuropsychologia, vol. 43, no. 7, pp. 989–1021, 2005.
[25]
S. Corkin, “Lasting consequences of bilateral medial temporal lobectomy: clinical course and experimental findings in H.M,” Seminars in Neurology, vol. 4, no. 2, pp. 249–259, 1984.
[26]
K. A. Paller and G. McCarthy, “Field potentials in the human hippocampus during the encoding and recognition of visual stimuli,” Hippocampus, vol. 12, no. 3, pp. 415–420, 2002.
[27]
G. Fernández, H. Weyerts, M. Schrader-B？lsche et al., “Successful verbal encoding into episodic memory engages the posterior hippocampus: a parametrically analyzed functional magnetic resonance imaging study,” Journal of Neuroscience, vol. 18, no. 5, pp. 1841–1847, 1998.
[28]
C. E. Stern, S. Corkin, R. G. González et al., “The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 16, pp. 8660–8665, 1996.
[29]
J. Poppenk, H. Evensmoen, M. Moscovitch, and L. Nadel, “Long-axis specialization of the human hippocampus,” Trends in Cognitive Sciences, vol. 17, no. 5, pp. 230–240, 2013.
[30]
A. Hupbach, O. Hardt, R. Gomez, and L. Nadel, “The dynamics of memory: context-dependent updating,” Learning and Memory, vol. 15, no. 8, pp. 574–579, 2008.
[31]
B. Jones, E. Bukoski, L. Nadel, and J. M. Fellous, “Remaking memories: reconsolidation updates positively motivated spatial memory in rats,” Learning & Memory, vol. 19, no. 3, pp. 91–98, 2012.
[32]
R. C. O'Reilly, R. Bhattacharyya, M. D. Howard, and N. Ketz, “Complementary learning systems,” Cognitive Science, pp. 1–20, 2011.
[33]
B. Aisa, B. Mingus, and R. O'Reilly, “The emergent neural modeling system,” Neural Networks, vol. 21, no. 8, pp. 1146–1152, 2008.
[34]
R. C. O'Reilly and Y. Munakata, Computational Explorations in Cognitive Neuroscience: Understanding the Mind By Simulating the Brain, The MIT Press, Cambridge, Mass, USA, 2000.
[35]
V. Cutsuridis, B. Graham, S. R. Cobb, and I. Vida, Hippocampal Microcircuits: A Computational Modelers' Resource Book, Springer, 2010.
[36]
E. J. Henriksen, L. L. Colgin, C. A. Barnes, M. P. Witter, M. B. Moser, and E. I. Moser, “Spatial representation along the proximodistal axis of CA1,” Neuron, vol. 68, no. 1, pp. 127–137, 2010.
[37]
G. Shepherd and S. Grillner, Handbook of Brain Microcircuits, Oxford Univ Press, Oxford, UK, 2010.
[38]
H. Hayashi and Y. Nonaka, “Cooperation and competition between lateral and medial perforant path synapses in the dentate gyrus,” Neural Networks, vol. 24, no. 3, pp. 233–246, 2011.
[39]
P. Poirazi, T. Brannon, and B. W. Mel, “Pyramidal neuron as two-layer neural network,” Neuron, vol. 37, no. 6, pp. 989–999, 2003.
[40]
P. B. Sederberg, M. W. Howard, and M. J. Kahana, “A context-based theory of recency and contiguity in free recall,” Psychological Review, vol. 115, no. 4, pp. 893–912, 2008.
[41]
S. M. Polyn, K. A. Norman, and M. J. Kahana, “A context maintenance and retrieval model of organizational processes in free recall,” Psychological Review, vol. 116, no. 1, pp. 129–156, 2009.
[42]
L. Nadel, The Hippocampus and Context Revisited, Hippocampal Place Fields. Oxford Scholarship Online Monographs, 2008.
[43]
T. Hafting, M. Fyhn, S. Molden, M. B. Moser, and E. I. Moser, “Microstructure of a spatial map in the entorhinal cortex,” Nature, vol. 436, no. 7052, pp. 801–806, 2005.
