Dynamics of spike transmission and suppression between principal cells and interneurons in the hippocampus and entorhinal cortex.

Synaptic excitation and inhibition are essential for neuronal communication. However, the variables that regulate synaptic excitation and inhibition in the intact brain remain largely unknown. Here, we examined how spike transmission and suppression between principal cells (PCs) and interneurons (INTs) are modulated by activity history, brain state, cell type, and somatic distance between presynaptic and postsynaptic neurons by applying cross-correlogram analyses to datasets recorded from the dorsal hippocampus and medial entorhinal cortex (MEC) of 11 male behaving and sleeping Long Evans rats. The strength, temporal delay, and brain-state dependency of the spike transmission and suppression depended on the subregions/layers. The spike transmission probability of PC-INT excitatory pairs that showed short-term depression versus short-term facilitation was higher in CA1 and lower in CA3. Likewise, the intersomatic distance affected the proportion of PC-INT excitatory pairs that showed short-term depression and facilitation in the opposite manner in CA1 compared with CA3. The time constant of depression was longer, while that of facilitation was shorter in MEC than in CA1 and CA3. During sharp-wave ripples, spike transmission showed a larger gain in the MEC than in CA1 and CA3. The intersomatic distance affected the spike transmission gain during sharp-wave ripples differently in CA1 versus CA3. A subgroup of MEC layer 3 (EC3) INTs preferentially received excitatory inputs from and inhibited MEC layer 2 (EC2) PCs. The EC2 PC-EC3 INT excitatory pairs, most of which showed short-term depression, exhibited higher spike transmission probabilities than the EC2 PC-EC2 INT and EC3 PC-EC3 INT excitatory pairs. EC2 putative stellate cells exhibited stronger spike transmission to and received weaker spike suppression from EC3 INTs than EC2 putative pyramidal cells. This study provides detailed comparisons of monosynaptic interaction dynamics in the hippocampal-entorhinal loop, which may help to elucidate circuit operations.

Cell type, sub-region, and layer-specific speed representation in the hippocampal-entorhinal circuit.

It has been hypothesised that speed information, encoded by 'speed cells', is important for updating spatial representation in the hippocampus and entorhinal cortex to reflect ongoing self-movement during locomotion. However, systematic characterisation of speed representation is still lacking. In this study, we compared the speed representation of distinct cell types across sub-regions/layers in the dorsal hippocampus and medial entorhinal cortex of rats during exploration. Our results indicate that the preferred theta phases of individual neurons are correlated with positive/negative speed modulation and a temporal shift of speed representation in a sub-region/layer and cell type-dependent manner. Most speed cells located in entorhinal cortex layer 2 represented speed prospectively, whereas those in the CA1 and entorhinal cortex layers 3 and 5 represented speed retrospectively. In entorhinal cortex layer 2, putative CA1-projecting pyramidal cells, but not putative dentate gyrus/CA3-projecting stellate cells, represented speed prospectively. Among the hippocampal interneurons, approximately one-third of putative dendrite-targeting (somatostatin-expressing) interneurons, but only a negligible fraction of putative soma-targeting (parvalbumin-expressing) interneurons, showed negative speed modulation. Putative parvalbumin-expressing CA1 interneurons and somatostatin-expressing CA3 interneurons represented speed more retrospectively than parvalbumin-expressing CA3 interneurons. These findings indicate that speed representation in the hippocampal-entorhinal circuit is cell-type, pathway, and theta-phase dependent.