Impulse responses distinguish two classes of directional motion-sensitive neurons in the nucleus of the optic tract

1. Recordings were made from direction-selective neurons in the nucleus of the optic tract (NOT) and dorsal terminal nucleus (DTN) of the wallaby, Macropus eugenii. Responses were elicited in the cells by brief displacements of a wide-field sine wave grating pattern in their preferred and antipreferred directions. The grating pattern was moved by a quarter cycle or less during the experiments. Once the stimulus duration was less than a certain value, referred to as the integration time, the magnitude of the responses depended on the size of the displacement, regardless of the velocity of the movement. The responses elicited by movements of the image in less than the integration times are referred to as velocity impulse responses. 2. The NOT-DTN contains two kinds of direction-selective neurons. The cells of the first type were maximally sensitive to patterns moving at low velocities (slow cells). These neurons had integration times of 40-80 ms. The cells of the second type were most sensitive to stimulus movements at high velocities (fast cells) and had integration times of 20-40 ms. 3. The velocity impulse responses of the slow cells were characterized by a rapid increase in firing rate followed by a slow exponential decline over a period of 1-4 s back to their resting activities. The impulse responses of the fast cells showed a rapid increase in firing rate followed by a short-lived inhibition of the background activity. 4. When the duration of the moving stimulus was longer than the integration times of the cells, they began to resolve the time course of the stimulus velocity. Under these conditions the slow cells showed a slow rise in firing rate during stimulation and a slow, exponential decay in firing after the stimulus came to rest. The fast cells showed a rapid increase in firing rate followed by a slow decay during the period of motion and then a short-lived inhibitory phase after the motion stopped. 5. The responses to rectangular pulses of stimulus velocity could be predicted for both cell types by convolving the velocity impulse responses of the cells with the velocity profile of the stimulus. Thus the cells responded linearly to image displacement in the sense that their responses to the velocity pulses could be described as the sum of a set of velocity impulse responses each weighted by the instantaneous stimulus strength, the latter being governed by the size of the image displacement. 6. Given the demonstration of linearity with respect to image displacement as the input, the Fourier transforms of the impulse responses were calculated to reveal the temporal filtering characteristics of the neurons. The slow cells had low-pass characteristics, the main power in the responses being at frequencies below 5-10 Hz. The fast cells had band-pass temporal filtering properties, the optimum pass band being at 6-12 Hz. 7. The filtering properties of the two cell types complement each other such that the optokinetic system as a whole is able to operate accurately over a wide frequency range.