Adaptation to visual motion in directional neurons of the nucleus of the optic tract.

Abstract

Extracellular recordings of action potentials were made from directional neurons in the nucleus of the optic tract (NOT) of the wallaby, Macropus eugenii, while stimulating with moving sine-wave gratings. When a grating was moved at a constant velocity in the preferred direction through a neuron's receptive field, the firing rate increased rapidly and then declined exponentially until reaching a steady-state level. The decline in response is called motion adaptation. The rate of adaptation increased as the temporal frequency of the drifting grating increased, up to the frequency that elicited the maximum firing rate. Beyond this frequency, the adaptation rate decreased. When the adapting grating's spatial frequency was varied, such that response magnitudes were significantly different, the maximum adaptation rate occurred at similar temporal frequencies. Hence the temporal frequency of the stimulus is a major parameter controlling the rate of adaptation. In most neurons, the temporal frequency response functions measured after adaptation were shifted to the right when compared with those obtained in the unadapted state. Further insight into the adaptation process was obtained by measuring the responses of the cells to grating displacements within one frame (10.23 ms). Such impulsive stimulus movements of less than a one-quarter cycle elicited a response that rose rapidly to a maximum and then declined exponentially to the spontaneous firing rate in several seconds. The level of adaptation was demonstrated by observing how the time constants of the exponentials varied as a function of the temporal frequency of a previously presented moving grating. When plotted as functions of adapting frequency, time constants formed a U-shaped curve. The shortest time constants occurred at similar temporal frequencies, regardless of changes in spatial frequency, even when the change in spatial frequency resulted in large differences in response magnitude during the adaptation period. The strongest adaptation occurred when the adapting stimulus moved in the neuron's preferred direction. Stimuli that moved in the antipreferred direction or flickered had an adapting influence on the responses to subsequent impulsive movements, but the effect was far smaller than that elicited by preferred direction adaptation. Adaptation in one region of the receptive field did not affect the responses elicited by subsequent stimulation in nonoverlapping regions of the field. Adaptation is a significant property of NOT neurons and probably acts to expand their temporal resolving power.