Increased excitatory synapse size in hippocampal place cells compared to silent cells

TL;DR

Hippocampal place cells have larger excitatory synapses than silent cells, suggesting synaptic plasticity supports spatial navigation.

Contribution

The study reveals that spine size differences, not overall spine density, correlate with place cell activity in hippocampal networks.

Findings

Place cells have significantly larger spine sizes compared to silent cells.

Excitatory synaptic plasticity may underlie the spatially tuned activity of hippocampal place cells.

Electrical and inhibitory synapse properties are similar across active and silent cells.

Abstract

Environment-specific neuronal activity in the hippocampus supports spatial navigation. A substantial fraction of pyramidal cells (PCs) is active whereas other neurons remain silent in a given environment across multiple days, suggesting that the allocation of neurons to a representation is a nonrandom process. Here, we report that PCs with different in vivo activities have similar electrical properties, inhibitory and excitatory synapse densities. However, our data revealed that the size of spines is significantly larger in place cells compared to silent cells. Our results are consistent with excitatory synaptic plasticity as a major mechanism underlying the different activities of hippocampal PCs in vivo.

Neuronal activity in the hippocampus creates a cognitive map of space that is essential for navigation. In any given environment, a fraction of hippocampal pyramidal cells (PCs) is active at specific locations (place cells), others are sparsely active without spatial tuning, and a significant proportion of the PCs is entirely silent. The mechanisms underlying the vastly different activities of PCs in the rodent hippocampal CA1 area are unknown. Here, we measured the in vivo activity of CA1 PCs using two-photon [Ca2+] imaging in head-restrained mice during navigation in a virtual corridor and then performed in vitro patch-clamp recording to probe their intrinsic electrical properties and anatomical investigation to characterize their input synapses. The active and passive electrical properties of PCs were similar between PCs with different prior in vivo activities. Perisomatic inhibitory synapse density was also comparable among PCs. The average dendritic spine density and spine head area did not correlate with the mean in vivo activity of PCs, but the size of the spines of place cells was significantly larger compared to that of silent cells. Our results are consistent with excitatory synaptic plasticity as a major mechanism underlying spatially tuned activity of place cells in hippocampal networks.

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