Hippocampal Anatomy Supports the Use of Context in Object Recognition: A Computational Model

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]  Jean-Marc Fellous,et al.  Remaking memories: reconsolidation updates positively motivated spatial memory in rats. , 2012, Learning & memory.

[2]  Emma R Wood,et al.  The role of the hippocampus in object recognition in rats: Examination of the influence of task parameters and lesion size , 2006, Behavioural Brain Research.

[3]  De Vries Book review: R.C. O'Reilly and Y. Munakata: Computational explorations in cognitive neuroscience: understanding the mind by stimulating the brain. Cambridge, Mass: The MIT Press. , 2002 .

[4]  R. O’Reilly,et al.  Computational Explorations in Cognitive Neuroscience: Understanding the Mind by Simulating the Brain , 2000 .

[5]  D. Amaral,et al.  Topographical organization of the entorhinal projection to the dentate gyrus of the monkey , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Michael S. Humphreys,et al.  A Context Noise Model of Episodic Recognition Memory , 2001 .

[7]  M. Moser,et al.  Pattern Separation in the Dentate Gyrus and CA3 of the Hippocampus , 2007, Science.

[8]  Jack W. Tsao,et al.  Handbook of brain microcircuits Gordon M. Shepherd , 2012, Journal of the Neurological Sciences.

[9]  Michael D. Howard,et al.  Complementary Learning Systems , 2014, Cogn. Sci..

[10]  Dave G. Mumby,et al.  Incidental (unreinforced) and reinforced spatial learning in rats with ventral and dorsal lesions of the hippocampus , 2009, Behavioural Brain Research.

[11]  Bartlett W. Mel,et al.  Pyramidal Neuron as Two-Layer Neural Network , 2003, Neuron.

[12]  T. Hafting,et al.  Microstructure of a spatial map in the entorhinal cortex , 2005, Nature.

[13]  Karim Nader,et al.  PKMζ maintains 1‐day‐ and 6‐day‐old long‐term object location but not object identity memory in dorsal hippocampus , 2009, Hippocampus.

[14]  H. Eichenbaum,et al.  What's new is older , 2013, eLife.

[15]  D. Mumby,et al.  Hippocampal damage and exploratory preferences in rats: memory for objects, places, and contexts. , 2002, Learning & memory.

[16]  R. Burwell The Parahippocampal Region: Corticocortical Connectivity , 2000, Annals of the New York Academy of Sciences.

[17]  R. Roesler,et al.  Temporary inactivation reveals an essential role of the dorsal hippocampus in consolidation of object recognition memory , 2006, Neuroscience Letters.

[18]  J. R. Baker,et al.  The hippocampal formation participates in novel picture encoding: evidence from functional magnetic resonance imaging. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Brian Mingus,et al.  The Emergent neural modeling system , 2008, Neural Networks.

[20]  B L McNaughton,et al.  Hippocampal granule cells opt for early retirement , 2010, Hippocampus.

[21]  Robert E. Clark,et al.  Impaired Recognition Memory in Rats after Damage to the Hippocampus , 2000, The Journal of Neuroscience.

[22]  A. Hupbach,et al.  The dynamics of memory: context-dependent updating. , 2008, Learning & memory.

[23]  R. O’Reilly,et al.  Conjunctive representations in learning and memory: principles of cortical and hippocampal function. , 2001, Psychological review.

[24]  C. Barnes,et al.  Spatial Representation along the Proximodistal Axis of CA1 , 2010, Neuron.

[25]  Hatsuo Hayashi,et al.  Cooperation and competition between lateral and medial perforant path synapses in the dentate gyrus , 2011, Neural Networks.

[26]  Mark Mayford,et al.  Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice , 2013, eLife.

[27]  J. Knierim,et al.  Major Dissociation Between Medial and Lateral Entorhinal Input to Dorsal Hippocampus , 2005, Science.

[28]  Sean M. Polyn,et al.  A context maintenance and retrieval model of organizational processes in free recall. , 2009, Psychological review.

[29]  Ken A Paller,et al.  Field potentials in the human hippocampus during the encoding and recognition of visual stimuli , 2002, Hippocampus.

[30]  M. Humphreys,et al.  A context noise model of episodic word recognition. , 2001, Psychological review.

[31]  M. Moser,et al.  Functional differentiation in the hippocampus , 1998, Hippocampus.

[32]  Michael R. Hunsaker,et al.  Dissociating the roles of dorsal and ventral CA1 for the temporal processing of spatial locations, visual objects, and odors. , 2008, Behavioral neuroscience.

[33]  Howard Eichenbaum,et al.  A cognitive map for object memory in the hippocampus. , 2009, Learning & memory.

[34]  Daniel L. Schacter,et al.  The case of K.C.: contributions of a memory-impaired person to memory theory , 2005, Neuropsychologia.

[35]  M. Witter Intrinsic and extrinsic wiring of CA3: indications for connectional heterogeneity. , 2007, Learning & memory.

[36]  Hallvard Røe Evensmoen,et al.  Long-axis specialization of the human hippocampus , 2013, Trends in Cognitive Sciences.

[37]  Susanna Sallstroem,et al.  Functional Differentiation , 2009, Modern Condensed Matter Physics.

[38]  S. Corkin Lasting Consequences of Bilateral Medial Temporal Lobectomy: Clinical Course and Experimental Findings in H.M. , 1984 .

[39]  C. B. Cave,et al.  Equivalent impairment of spatial and nonspatial memory following damage to the human hippocampus , 1991, Hippocampus.

[40]  Marc W Howard,et al.  A context-based theory of recency and contiguity in free recall. , 2008, Psychological review.

[41]  G. Mangun,et al.  Successful Verbal Encoding into Episodic Memory Engages the Posterior Hippocampus: A Parametrically Analyzed Functional Magnetic Resonance Imaging Study , 1998, The Journal of Neuroscience.

[42]  E. Rolls,et al.  Computational analysis of the role of the hippocampus in memory , 1994, Hippocampus.

[43]  Bruce P. Graham,et al.  Comprar Hippocampal Microcircuits · A Computational Modeler's Resource Book | Cutsuridis, Vassilis | 9781441909954 | Springer , 2010 .

[44]  Michael R. Hunsaker,et al.  Dissociations of the medial and lateral perforant path projections into dorsal DG, CA3, and CA1 for spatial and nonspatial (visual object) information processing. , 2007, Behavioral neuroscience.

[45]  L. Squire,et al.  Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.