A novel somatosensory spatial navigation system outside the hippocampal formation

Abstract

Spatially selective firing of place cells, grid cells, boundary vector/border cells and head direction cells constitutes the basic building blocks of a canonical spatial navigation system centered on the hippocampal-entorhinal complex. While head direction cells can be found throughout the brain, spatial tuning outside the hippocampal formation is often non-specific or conjunctive to other representations such as a reward. Although the precise mechanism of spatially selective firing activity is not understood, various studies show sensory inputs, particularly vision, heavily modulate spatial representation in the hippocampal-entorhinal circuit. To better understand the contribution of other sensory inputs in shaping spatial representation in the brain, we performed recording from the primary somatosensory cortex in foraging rats. To our surprise, we were able to detect the full complement of spatially selective firing patterns similar to that reported in the hippocampal-entorhinal network, namely, place cells, head direction cells, boundary vector/border cells, grid cells and conjunctive cells, in the somatosensory cortex. These newly identified somatosensory spatial cells form a spatial map outside the hippocampal formation and support the hypothesis that location information modulates body representation in the somatosensory cortex. Our findings provide transformative insights into our understanding of how spatial information is processed and integrated in the brain, as well as functional operations of the somatosensory cortex in the context of rehabilitation with brain-machine interfaces.

Fig. 1. Place cells in the somatosensory cortex.

a A Nissl-stained coronal section (top) showing tetrode tracking trajectory (arrowheads) through all of six layers across the rat primary somatosensory cortex. Dashed lines depict the boundaries of the hindlimb (S1HL) and shoulder (S1Sh) regions of the primary somatosensory cortex (S1). The bottom panel shows the schematic delimitation of the different layers and sub-regions of the primary somatosensory cortex. Scale bar, 1 mm. b Trajectory (gray line) with superimposed spike locations (red dots) (left column); heat maps of spatial firing rate (middle left column) and autocorrelation (middle right column) are color-coded with dark blue indicating minimal firing rate and dark red indicating maximal firing rate. The scale of the autocorrelation is twice the scale of the spatial firing rate maps. Peak firing rate (fr), mean firing rate (fr) and spatial information (si) for each representative cell are labeled on the top of the panels. Spike waveforms on four electrodes are shown on the right column. Scale bar, 150 µV, 300 µs. The zero microvolt horizontal baseline is drawn with the orange dashed lines for the spike waveforms on all four electrodes. c Distribution of within-cell shuffled spatial information for three representative somatosensory place cells. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. The red line indicates the observed spatial information. d Distribution of spatial information for all isolated somatosensory units. The top panel shows the distribution for observed spatial information. The bottom panel shows the distribution for randomly shuffled data from the same sample. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. A zoomed panel shows the magnification of the specified area marked by the red dashed rectangle. e The uniformly areal distribution of various place firing fields relative to the field center. f–h The population histograms of place firing field sizes (f), spatial coherence (g) and spatial sparsity (h) for all of 195 identified somatosensory place cells.

Fig. 2. Head direction cells recorded from the somatosensory cortex.

a Three examples of somatosensory head direction cells. Trajectory (gray line) with superimposed spike locations (red dots) (left column); spatial firing rate maps (middle left column), autocorrelation diagrams (middle right column) and head direction tuning curves (black) plotted against dwell-time polar plot (gray) (right column). Firing rate is color-coded with dark blue indicating minimal firing rate and dark red indicating maximal firing rate. The scale of the autocorrelation is twice the scale of the spatial firing rate maps. Peak firing rate (fr), mean firing rate (fr), mean vector length (mvl) and angular peak rate for each representative head direction cell are labeled on the top of the panels. The directional plots show strong head direction tuning. Spike waveforms on four electrodes are shown on the right column. The zero microvolt horizontal baseline is drawn with the orange dashed lines for the spike waveforms on all four electrodes. Scale bar, 150 µV, 300 µs. b Distribution of within-cell shuffled mean vector length for three representative somatosensory head direction cells. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. The purple line indicates the observed mean vector length. c Distribution of mean vector length for all identified somatosensory units. The top panel shows the distribution for observed values. The bottom panel shows the distribution for randomly shuffled data from the same sample. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. The insets show the magnification of the specified area marked by the purple dashed rectangle. d Distribution of head directional tuning width. e Preferred direction of recorded head direction cells from S1. The polar plot shows the distribution of the peak firing direction of all identified somatosensory head direction cells. The preferred head direction exhibits a uniform distribution (P = 0.08, Rayleigh’s test).

Fig. 3. Border cells recorded from the somatosensory cortex.

a Three representative examples of somatosensory border cells. Trajectory (gray line) with superimposed spike locations (red dots) (left column); heat maps of spatial firing rate (middle column) and autocorrelation diagrams (right column). Firing rate is color-coded with dark blue indicating minimal firing rate and dark red indicating maximal firing rate. The scale of the autocorrelation is twice the scale of the spatial firing rate maps. Peak firing rate (fr), mean firing rate (fr) and border score (b) for each representative border cell are labeled on the top of the panels. Spike waveforms on four electrodes are shown on the right column. The zero microvolt horizontal baseline is drawn with the orange dashed lines for the spike waveforms on all four electrodes. Scale bar, 150 µV, 300 µs. b Distribution of within-cell shuffled border score for three representative somatosensory border cells. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. The green line indicates the observed border score. c Distribution of border scores for pooled somatosensory cells. The top panel shows the distribution for observed values. The bottom panel shows the distribution for randomly shuffled versions from the same sample. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. A zoomed panel shows the magnification of the specified area marked by the green dashed rectangle.

Fig. 4. Grid cells in the somatosensory cortex.

a Three representative examples of somatosensory grid cells. Trajectory (gray line) with superimposed spike locations (red dots) (left column); heat maps of spatial firing rate (middle column) and autocorrelation diagrams (right column). Firing rate is color-coded with dark blue indicating minimal firing rate and dark red indicating maximal firing rate. The scale of the autocorrelation is twice the scale of the spatial firing rate maps. Peak firing rate (fr), mean firing rate (fr) and grid score (g) for each representative grid cell are labeled on the top of the panels. A crystal-like hexagonal firing pattern was observed. Spike waveforms on four electrodes are shown on the right column. The zero microvolt horizontal baseline is drawn with the orange dashed lines for the spike waveforms on all four electrodes. Scale bar, 100 µV, 300 µs. b Distribution of within-cell shuffled grid score for three representative somatosensory grid cells. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. The cyan line indicates the observed grid score. c The same as (b) but for field shuffle. d Distribution of grid scores for somatosensory cells. The top panel shows the distribution for observed values. The bottom panel shows the distribution for randomly shuffled versions from the same sample. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. Insets show the magnification of the specified area marked by the cyan dashed rectangle. e, f The raster plots show the distribution of grid spacing and grid size of the classified somatosensory grid cells. g The histogram of grid orientation from categorized somatosensory grid cells. h Three representative examples of irregular somatosensory grid cells. Spike waveforms on four electrodes are shown on the right column. Scale bar, 150 µV, 300 µs.

Fig. 5. Four different types of conjunctive cells in the somatosensory cortex.

a A representative conjunctive place-by-head direction cell. b A representative conjunctive border-by-head direction cell. c A representative conjunctive grid-by-head direction cell. d A representative conjunctive irregular grid-by-head direction cell. Trajectory (gray line) with superimposed spike locations (red dots) (left column); heat maps of spatial firing rate (middle left column), autocorrelation diagrams (middle right column) and head direction tuning curves (black) plotted against dwell-time polar plot (gray) (right column). Firing rate is color-coded with dark blue indicating minimal firing rate and dark red indicating maximal firing rate. The scale of the autocorrelation is twice the scale of the spatial firing rate maps. Peak firing rate (fr), mean firing rate (fr), spatial information (si), border score (b), grid score (g) and mean vector length (mvl) for each representative cell are labeled on the top of the panels. Spike waveforms on four electrodes are shown on the right column. The zero microvolt horizontal baseline is drawn with the orange dashed lines for the spike waveforms on all four electrodes. Scale bar, 150 µV, 300 µs.

Fig. 6. Somatosensory spatial response after whisker-trimming.

a–d Four representative examples of somatosensory place cell (a), head direction cell (b), border cell (c) and grid cell (d) after whisker-trimming. Trajectory (gray line) with superimposed spike locations (red dots) (left column); spatial firing rate maps (middle left column), autocorrelation diagrams (middle right column) and head direction tuning curves (black) plotted against dwell-time polar plot (gray) (right column). Firing rate is color-coded with dark blue indicating minimal firing rate and dark red indicating maximal firing rate. The scale of the autocorrelation is twice the scale of the spatial firing rate maps. Peak firing rate (fr), mean firing rate (fr), spatial information (si), mean vector length (mvl), border score (b) or grid score (g) and angular peak rate for each representative cell are labeled on the top of the panels. Spike waveforms on four electrodes are shown on the right column. The zero microvolt horizontal baseline is drawn with the orange dashed lines for the spike waveforms on all four electrodes. Scale bar, 150 µV, 300 µs. e–h Distribution of spatial information (e), mean vector length (f), border score (g) or grid score (h) for somatosensory cells after whisker-trimming. The top panel shows the distribution for observed values. The bottom panel shows the distribution for randomly shuffled data from the same sample. The orange and blue stippled lines mark the 99th and the 95th percentile significance level of each randomly shuffled distribution, respectively. A zoomed panel shows the magnification of the specified area marked by the dark red dashed rectangle.