Abstract
SummaryGrid cells are spatially modulated neurons within the medial entorhinal cortex whose firing fields are arranged at the vertices of tessellating equilateral triangles [1]. The exquisite periodicity of their firing has led to the suggestion that they represent a path integration signal, tracking the organism’s position by integrating speed and direction of movement [2, 3, 4, 5, 6, 7, 8, 9, 10]. External sensory inputs are required to reset any errors that the path integrator would inevitably accumulate. Here we probe the nature of the external sensory inputs required to sustain grid firing, by recording grid cells as mice explore familiar environments in complete darkness. The absence of visual cues results in a significant disruption of grid cell firing patterns, even when the quality of the directional information provided by head direction cells is largely preserved. Darkness alters the expression of velocity signaling within the entorhinal cortex, with changes evident in grid cell firing rate and the local field potential theta frequency. Short-term (<1.5 s) spike timing relationships between grid cell pairs are preserved in the dark, indicating that network patterns of excitatory and inhibitory coupling between grid cells exist independently of visual input and of spatially periodic firing. However, we find no evidence of preserved hexagonal symmetry in the spatial firing of single grid cells at comparable short timescales. Taken together, these results demonstrate that visual input is required to sustain grid cell periodicity and stability in mice and suggest that grid cells in mice cannot perform accurate path integration in the absence of reliable visual cues.
Highlights
In order to determine the importance of visual cues in supporting grid cell firing, we recorded 277 grid cells from the medial entorhinal cortex after mice were introduced into a familiar environment in total darkness
In the absence of visual cues, the characteristic periodicity of grid cells was disrupted and gridness scores were considerably reduced compared to the baseline light trials (Figures 1B and S1A; 2 3 2 ANOVA, main effect of light condition, N = 277, F1,275 = 954.22, p < 0.001)
Spatial information scores in darkness did not improve upon repeated exposures to the dark condition, despite increases in baseline spatial information scores in the light (Figures 1C and S1B; 2 3 2 ANOVA experience, F1,275 = 8.8, p = 0.03; light 3 experience, F1,275 = 12.8, p < 0.001; simple main effects [SME] experience(light), p = 0.001; SME experience(dark), p = 0.167); while intra-trial stability increased slightly after repeated exposures, in both light and dark (Figures 1D and S1C; 2 3 2 ANOVA experience, F1,275 = 47.7, p < 0.001; light 3 experience, F1,275 = 3.49, p = 0.063)
Summary
To establish whether eliminating visual input disrupts grid firing even when a continuous stream of self-motion information is available, we introduced mice to the familiar environment with the lights on and turned the lights off 10 min after the start of the trial (light-dark condition; Figures S1O–S1Y). There was no significant improvement over the dark condition: gridness was still significantly lower during the dark phase of the trial compared to the light phase (Figure S1Q; 2 3 2 ANOVA, main effect of light condition, F1,346 = 835.33, p < 0.001). After several exposures to the light-dark condition (n R 4 exposures), gridness values slightly improved, with some regularity appearing in the firing-rate maps (light 3 experience, F1, 346 = 37.3, p < 0.001; SME experience(dark), p = 0.006; see Figures S1Q– S1S for further quantification)
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