Neuron
Volume 95, Issue 3, 2 August 2017, Pages 656-672.e3
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Article
Proximodistal Heterogeneity of Hippocampal CA3 Pyramidal Neuron Intrinsic Properties, Connectivity, and Reactivation during Memory Recall

https://doi.org/10.1016/j.neuron.2017.07.012Get rights and content
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Highlights

  • CA3 shows a marked proximodistal gradient in intrinsic and synaptic properties

  • Mossy fiber and direct cortical inputs show opposing gradients of synaptic strength

  • CA3b has the strongest recurrent excitation because of reduced inhibition

  • This connectivity can explain robust CA3b reactivation during fear memory retrieval

Summary

The hippocampal CA3 region is classically viewed as a homogeneous autoassociative network critical for associative memory and pattern completion. However, recent evidence has demonstrated a striking heterogeneity along the transverse, or proximodistal, axis of CA3 in spatial encoding and memory. Here we report the presence of striking proximodistal gradients in intrinsic membrane properties and synaptic connectivity for dorsal CA3. A decreasing gradient of mossy fiber synaptic strength along the proximodistal axis is mirrored by an increasing gradient of direct synaptic excitation from entorhinal cortex. Furthermore, we uncovered a nonuniform pattern of reactivation of fear memory traces, with the most robust reactivation during memory retrieval occurring in mid-CA3 (CA3b), the region showing the strongest net recurrent excitation. Our results suggest that heterogeneity in both intrinsic properties and synaptic connectivity may contribute to the distinct spatial encoding and behavioral role of CA3 subregions along the proximodistal axis.

Keywords

Hippocampus
CA3
CA2
recurrent collateral
mossy fiber
intrinsic excitability
input resistance
perforant path
pattern completion
contextual fear conditioning

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