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Previous studies have shown that a subset of neurons in the rat anterodorsal thalamus discharge as a function of the animal's head direction (HD) in the horizontal plane, independent of the animal's location and behavior. These cells have consistent firing properties across a wide range of conditions and cell discharge appears highly regular when listened to through a loudspeaker. In contrast, interspike interval (ISI) analyses on cortical cells have found that cell firing is irregular, even under constant stimulus conditions. Here, we analyzed HD cells from the anterodorsal thalamus, while rats foraged for food pellets, to determine whether their firing was regular or irregular. ISIs were measured when the animal's HD was maintained within ± 6° of the cell's preferred firing direction. ISIs were highly variable with a mean coefficient of variation (CV) of 0.681. For each cell, the CV values at HDs ± 24° away from the cell's preferred direction were similar to the coefficient measured at the cell's preferred direction. A second recording session showed that cells had similar coefficients of variation as the first session, suggesting that the degree of variability in cell spiking was a characteristic property for each cell. There was little correlation between ISIs and angular head velocity or translational speed. ISIs measured in HD cells from the postsubiculum and lateral mammillary nuclei showed higher CV values. These results indicate that despite the appearance of regularity in their firing, HD cells, like cortical cells, have irregular ISIs. In contrast to the irregular firing observed for ISIs, analyses over longer time intervals indicated that HD cell firing was much more regular, more nearly resembling a rate code. These findings have implications for attractor networks that model the HD signal and for models proposed to explain the generation of grid cell signals in entorhinal cortex.

Interspike Interval Analyses Reveal Irregular Firing Patterns at Short, But Not Long, Intervals in Rat Head Direction Cells