TY - JOUR
T1 - Tracking the flow of hippocampal computation
T2 - Pattern separation, pattern completion, and attractor dynamics
AU - Knierim, James J.
AU - Neunuebel, Joshua P.
N1 - Funding Information:
We thank I. Lee, D. Yoganarasimha, F. Savelli, and G. Rao for help in data collection for some of the figures shown in this manuscript. The experiments reviewed here were supported by Public Health Service grants NS039456 and MH094146 and by the Johns Hopkins University Brain Sciences Institute . The funding agency had no role in the design, data collection, analysis, or writing of the paper.
Publisher Copyright:
© 2015 Elsevier Inc..
PY - 2016/3/1
Y1 - 2016/3/1
N2 - Classic computational theories of the mnemonic functions of the hippocampus ascribe the processes of pattern separation to the dentate gyrus (DG) and pattern completion to the CA3 region. Until the last decade, the large majority of single-unit studies of the hippocampus in behaving animals were from the CA1 region. The lack of data from the DG, CA3, and the entorhinal inputs to the hippocampus severely hampered the ability to test these theories with neurophysiological techniques. The past ten years have seen a major increase in the recordings from the CA3 region and the medial entorhinal cortex (MEC), with an increasing (but still limited) number of experiments from the lateral entorhinal cortex (LEC) and DG. This paper reviews a series of studies in a local-global cue mismatch (double-rotation) experiment in which recordings were made from cells in the anterior thalamus, MEC, LEC, DG, CA3, and CA1 regions. Compared to the standard cue environment, the change in the DG representation of the cue-mismatch environment was greater than the changes in its entorhinal inputs, providing support for the theory of pattern separation in the DG. In contrast, the change in the CA3 representation of the cue-mismatch environment was less than the changes in its entorhinal and DG inputs, providing support for a pattern completion/error correction function of CA3. The results are interpreted in terms of continuous attractor network models of the hippocampus and the relationship of these models to pattern separation and pattern completion theories. Whereas DG may perform an automatic pattern separation function, the attractor dynamics of CA3 allow it to perform a pattern separation or pattern completion function, depending on the nature of its inputs and the relative strength of the internal attractor dynamics.
AB - Classic computational theories of the mnemonic functions of the hippocampus ascribe the processes of pattern separation to the dentate gyrus (DG) and pattern completion to the CA3 region. Until the last decade, the large majority of single-unit studies of the hippocampus in behaving animals were from the CA1 region. The lack of data from the DG, CA3, and the entorhinal inputs to the hippocampus severely hampered the ability to test these theories with neurophysiological techniques. The past ten years have seen a major increase in the recordings from the CA3 region and the medial entorhinal cortex (MEC), with an increasing (but still limited) number of experiments from the lateral entorhinal cortex (LEC) and DG. This paper reviews a series of studies in a local-global cue mismatch (double-rotation) experiment in which recordings were made from cells in the anterior thalamus, MEC, LEC, DG, CA3, and CA1 regions. Compared to the standard cue environment, the change in the DG representation of the cue-mismatch environment was greater than the changes in its entorhinal inputs, providing support for the theory of pattern separation in the DG. In contrast, the change in the CA3 representation of the cue-mismatch environment was less than the changes in its entorhinal and DG inputs, providing support for a pattern completion/error correction function of CA3. The results are interpreted in terms of continuous attractor network models of the hippocampus and the relationship of these models to pattern separation and pattern completion theories. Whereas DG may perform an automatic pattern separation function, the attractor dynamics of CA3 allow it to perform a pattern separation or pattern completion function, depending on the nature of its inputs and the relative strength of the internal attractor dynamics.
KW - Attractors
KW - CA3
KW - Dentate gyrus
KW - Pattern completion
KW - Pattern separation
KW - Place cells
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U2 - 10.1016/j.nlm.2015.10.008
DO - 10.1016/j.nlm.2015.10.008
M3 - Review article
C2 - 26514299
AN - SCOPUS:84960309242
SN - 1074-7427
VL - 129
SP - 38
EP - 49
JO - Neurobiology of Learning and Memory
JF - Neurobiology of Learning and Memory
ER -