The Irregular Firing Properties of Thalamic Head Direction Cells

23 Head-direction cells encode an animal’s heading in the horizontal plane. However, it is not 24 clear why the directionality of a cell’s mean firing rate differs for clockwise, compared to 25 counter-clockwise head turns (this difference is known as the ‘separation angle’) in anterior 26 thalamus. Here we investigated, in freely-behaving rats, if intrinsic neuronal firing properties 27 are linked to this phenomenon. We found a positive correlation between the separation angle 28 and the spiking variability of thalamic head-direction cells. To test whether this link is driven 29 by hyperpolarisation-inducing currents, we investigated the effect of thalamic reticular 30 inhibition during high-voltage spindles on directional spiking. While the selective directional 31 firing of thalamic neurons was preserved, we found no evidence for entrainment of thalamic 32 head-direction cells by high-voltage spindle oscillations. We then examined the role of 33 depolarisation-inducing currents in the formation of separation angle. Using a single34 compartment Hodgkin–Huxley model, we show that modelled neurons fire with higher 35 frequencies during the ascending phase of sinusoidal current injection (mimicking the head36 direction tuning curve), when simulated with higher high-threshold calcium channel 37 conductance. These findings demonstrate that the turn-specific encoding of directional signal 38 strongly depends on the ability of thalamic neurons to fire irregularly in response to 39 sinusoidal excitatory activation. Another crucial factor for inducing phase lead to sinusoidal 40 current injection was the presence of spike-frequency adaptation current in the modelled 41 neurons. Our data support a model in which intrinsic biophysical properties of thalamic 42 neurons mediate the physiological encoding of directional information. 43