Abstract
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.
Highlights
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
To compare the correlation between firing rate and running speed in distinct cell types, recorded neurons were first classified as either principal neurons or interneurons based on spike waveforms and the physiological criteria outlined in previous studies[57,58,61,62,63,64]
In order to understand how speed information is handled in the hippocampal–entorhinal circuit, we compared the speed representation of distinct cell types across different sub-regions and layers of the hippocampus and medial entorhinal cortex (MEC)
Summary
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. 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. Spatially modulated cells in the superficial layers of the MEC show anticipatory firing field shifts between high and low speeds, and between positive and negative accelerations that increase with the absolute acceleration threshold[10]. This observation is consistent with the notion that the activity of spatially modulated cells in the superficial MEC is driven by speed cells with prospective coding[10]. The information encoded by speed cells may be utilised to optimise coding in the MEC because the neurons therein vary their coding properties dynamically in such a way that they become more informative about position, head direction, and the conjunction of position and head direction when an animal is running at higher speeds[26]
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