The irregular firing properties of thalamic head direction cells mediate turn-specific modulation of the directional tuning curve.

Abstract

HEAD DIRECTION (HD) cells in anterior thalamus express a wide range of interspike intervals (ISIs) (Taube 2010). Given the importance of HD encoding for spatial navigation in the environment, it is crucial to understand whether intrinsic biophysical properties mediate the shape of directional tuning curves. Here we ask how ISI patterns affect the formation of the HD tuning curve in the horizontal plane. ISI variability is evaluated by the coefficient of variation; high values reflect an irregular pattern of the spikes (Softky and Koch 1993). ISI variability is very sensitive to the mean firing rate (Holt et al. 1996; Softky and Koch 1993); however, large ISIs as part of intertrain analyses are not simply noise around the mean firing rate but reflect characteristics of the membrane potential (Angelo and Margrie 2011). To investigate the functional relation between ISI diversity and separation angle, we use a single-cell Hodgkin-Huxley-type model to simulate ISI patterns ranging from irregularly to regularly firing-type cells (Pospischil et al. 2008). We apply sinusoidal current injection that mimics the Gaussian distribution of HD signal in thalamic neurons (Taube et al. 1990). Experimental and theoretical evidence suggests that bursts occur preferentially on the ascending slope of input signal (Gabbiani et al. 1996; Guido et al. 1992; Kepecs et al. 2002). Thus irregularly spiking neurons may detect the rising slope of input signals with greater precision compared with regularly spiking neurons (Metzner et al. 1998; Sherman 2001).