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.

. Number of cells analysed, and numbers and proportions of p-Speed, n-Speed, and non-speed cells. . Relationship between spatial information per spike (bits/spike) and speed score.
Spatial information per spike (bits/spike) and speed score of individual neurons are shown. Principal neurons (top) and interneurons (bottom) of CA1, CA3, EC2, EC3, and EC5 are shown separately. r, correlation coefficient between spatial information per spike (bits/spike) and speed score. r(abs), correlation coefficient between spatial information per spike (bits/spike) and absolute value of speed score. * P < 0.05, ** P < 0.01, **** P < 0.0001. n.s., the correlation between spatial information per spike (bits/spike) and speed score is not statistically significant. n.s. (abs), the correlation between spatial information per spike (bits/spike) and absolute value of speed score is not significant. Red, p-Speed cells (pos); Blue, n-Speed cells (neg); Yellow, non-speed cells (ns). Consistent with the previous study 1 , overall we observed that spatial information per spike (bits/spike) and (absolute value of) speed score were negatively correlated. Figure S2. Relationship between spatial information per second (bits/s) and speed score.
Spatial information per second (bits/s) and speed score of individual neurons are shown. Principal neurons (top) and interneurons (bottom) of CA1, CA3, EC2, EC3, and EC5 are shown separately. r, correlation coefficient between spatial information per second (bits/s) and speed score. r(abs), correlation coefficient between spatial information per second (bits/s) and absolute value of speed score. * P < 0.05, *** P < 0.001, **** P < 0.0001. n.s., the correlation between spatial information per second (bits/s) and speed score is not significant. n.s. (abs), the correlation between spatial information per second (bits/s) and absolute value of speed score is not significant. Red, p-Speed cells (pos); Blue, n-Speed cells (neg); Yellow, non-speed cells (ns). Overall, we found that spatial information per second (bits/s) and (absolute value of) speed score positively correlated. The discrepancy between the relationship between spatial information per spike (bits/spike) vs speed score (Fig. S1) and the relationship between spatial information per second (bits/s) vs  coefficient between directional information per spike (bits/spike) and speed score. r(abs), correlation coefficient between directional information per spike (bits/spike) and absolute value of speed score. * P < 0.05, ** P < 0.01, *** P < 0.001, **** P < 0.0001. n.s., the correlation between directional information (bits/spike) and speed score is not significant. n.s. (abs), the correlation between directional information per spike (bits/spike) and absolute value of speed score is not significant. Red, p-Speed cells (pos); Blue, n-Speed cells (neg); Yellow, non-speed cells (ns). Consistent with the previous study reporting the relationship between head direction score and speed score 1 , overall we found that directional information per spike (bits/spike) and (absolute value of) speed score negatively correlated.  score and speed score. r(abs), correlation coefficient between gridness score and absolute value of speed score.
(abs), the correlation between gridness score and absolute value of speed score is not significant. Red, p-Speed cells (pos); Blue, n-Speed cells (neg); Yellow, non-speed cells (ns). Table S2. Speed score of p-Speed cells.
Means and standard deviations of speed score are summarised.
Principal neurons and interneurons in each region (same data as in Fig. 4a,

Speed slope [Hz/(cm/s)]
Principal neurons and interneurons in each region (same data as in Fig. 4c, Table S4. Speed information of p-Speed cells. Means and standard deviations of speed information per second (bits/s) and speed information per spike (bits/spike) are summarised.

Speed information per second (bits/s)
Principal neurons and interneurons in each region (same data as in Fig. 4g