Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input

Abstract

Vestibular information influences spatial orientation and navigation in laboratory animals and humans. Neurons within the rat anterior thalamus encode the directional heading of the animal in absolute space. These neurons, referred to as head direction (HD) cells, fire selectively when the rat points its head in a specific direction in the horizontal plane with respect to the external laboratory reference frame. HD cells are thought to represent an essential component of a neural network that processes allocentric spatial information. The functional properties of HD cells may be dependent on vestibular input. Here, anterior thalamic HD cells were recorded before and after sodium arsanilate-induced vestibular system lesion. Vestibular lesions abolished the directional firing properties of HD cells. The time course of disruption in the directional firing properties paralleled the loss of vestibular function. Arsanilate-treated rats exhibited only minor changes in locomotor behavior, which were unlikely to account for the loss of direction-specific firing. Vestibular lesions also disrupted the influence of angular head velocity on anterior thalamic single-unit firing rates. Finally, a subset of anterior thalamic neurons recorded from vestibular-lesioned rats exhibited a pattern of intermittent firing bursts that were distinctly unrelated to HD. This novel anterior thalamic firing pattern has not been encountered in any vestibular-intact rat. These data suggest that: (1) the neural code for directional bearing is critically dependent on vestibular information; and (2) this loss of HD cell information may represent a neurobiological mechanism to account for the orientation and navigational deficits observed after vestibular dysfunction.