Degradation of Head Direction Cell Activity during Inverted Locomotion

Representative firing rate × HD tuning curves across each of the four surfaces. HD is shown on the abscissa, the firing rate is plotted as a solid line relative to the left ordinate, and the number of samples at each directional bin is plotted as a dotted line relative to the right ordinate using a logarithmic scale. A, Tuning curves from three different HD cells categorized as CD. Note the present but degraded directional specificity while the animal was traversing the ceiling in an inverted orientation. B, Tuning curves from three HD cells categorized as CND. Note the absence of directional specificity while the animal was traversing the ceiling. Plots are constructed using 6° directional bins. deg., Degree.

Firing rate × HD × time plot for two consecutive trials. Time is represented on the abscissa with the distance between tic marks indicating 5 s. The HD of the animal is indicated as a dotted gray line using the left ordinate, whereas the firing rate of the recorded cell is plotted as the black line on the right ordinate. The label under each panel indicates the current surface being traversed and the general direction of locomotion relative to the preferred direction of the cell. This cell had a preferred direction of ∼0° (east). Note the influence of HD on the firing rate on the floor and when the animal ascends and descends the walls (compare panels labeled preferred and nonpreferred). In contrast, when the animal was locomoting on the ceiling, the firing rate of the cell was generally not affected by HD. The firing rate trace was smoothed by averaging each value across five points forward and backward in time. The HD trace was not smoothed. deg., Degree.

Frequency distributions of mean vector lengths obtained from Rayleigh analysis of directional tuning. Mean vector length is a measure of directional specificity, with increasing values indicating cellular activity dependent on the HD of the animal. The filled bars indicate cells showing significant (p < 0.05) directional specificity on that surface, whereas the open bars indicate cells failing to show directional specificity on that surface.

Firing rate × HD tuning curve of a representative HD cell plotted as a function of whether the animal was ascending a wall, locomoting inverted across the ceiling, or descending a wall. Note that the directional specificity is maintained when the animal descended, although the cell was nondirectional on the ceiling. deg., Degree.

Scatter diagrams showing the amount of angular shift of preferred directions between different surfaces. While traversing the walls, cells tended to show preferred directions similar to the floor (top row). In contrast, preferred directions tended to shift randomly while the animal was locomoting in an inverted position (bottom left panel). Cells showed stable tuning when the east and west compartments of the floor surface are compared (bottom right panel). The angular position of each filled circle represents the shift of preferred direction for individual cells between the two surfaces. For each comparison, only angular shifts from the cells showing maintenance of directional tuning on both surfaces are shown. The dotted arrow denotes an angular shift of zero, and the solid arrow denotes the observed mean vector angle. The length of the solid arrow denotes the mean vector length; a length of 1.0 (no variability in shift scores) is represented by a vector spanning the radius of the circle.