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Neural Population Evidence of Functional Heterogeneity along the CA3 Transverse Axis: Pattern Completion versus Pattern Separation

Classical theories of associative memory model CA3 as a homogeneous attractor network because of its strong recurrent circuitry. However, anatomical gradients suggest a functional diversity along the CA3 transverse axis. We examined the neural population coherence along this axis, when the local and...

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Published in:Neuron (Cambridge, Mass.) Mass.), 2015-09, Vol.87 (5), p.1093-1105
Main Authors: Lee, Heekyung, Wang, Cheng, Deshmukh, Sachin S., Knierim, James J.
Format: Article
Language:English
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Summary:Classical theories of associative memory model CA3 as a homogeneous attractor network because of its strong recurrent circuitry. However, anatomical gradients suggest a functional diversity along the CA3 transverse axis. We examined the neural population coherence along this axis, when the local and global spatial reference frames were put in conflict with each other. Proximal CA3 (near the dentate gyrus), where the recurrent collaterals are the weakest, showed degraded representations, similar to the pattern separation shown by the dentate gyrus. Distal CA3 (near CA2), where the recurrent collaterals are the strongest, maintained coherent representations in the conflict situation, resembling the classic attractor network system. CA2 also maintained coherent representations. This dissociation between proximal and distal CA3 provides strong evidence that the recurrent collateral system underlies the associative network functions of CA3, with a separate role of proximal CA3 in pattern separation. •Neural population analyses reveal functional dissociation along CA3 transverse axis•Proximal CA3 population activity demonstrates computational pattern separation•Distal CA3 population activity demonstrates computational pattern completion•CA2 population activity is similar to distal CA3 in a cue-mismatch environment Lee et al. show that there is functional heterogeneity along the CA3 transverse axis of the hippocampus. In a cue-mismatch environment, proximal CA3 demonstrated pattern separation, and distal CA3 demonstrated pattern completion.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2015.07.012