Spatiotemporal response properties of direction-selective neurons in the nucleus of the optic tract and dorsal terminal nucleus of the wallaby, Macropus eugenii

1. The spatial and temporal response characteristics of direction- selective neurons in the nucleus of the optic tract and dorsal terminal nucleus of the accessory optic system (NOT-DTN) of the wallaby were established using moving sinusoidal gratings. This is the first comprehensive investigation of the spatiotemporal response characteristics of NOT-DTN neurons in any species. 2. The analysis revealed two main classes of cells. The first class, referred to as slow neurons, are maximally sensitive to mo- tion at low temporal frequencies (<1 Hz) and high spatial frequencies (0.5- 1.0 cpd). The second class, referred to as fast neurons, are most sensitive to motion at high temporal frequencies (> 10 Hz) and moderate to low spatial frequencies (0.1-0.5 cpd). The fast neurons also have a domain of high sensitivity at low temporal frequencies and high spatial frequencies. As the neurons are tuned to specific temporal frequencies of motion, rather than image velocities, it is suggested that the motion detectors are of the delay- and-compare type and code local motion-related changes in contrast or luminance. 3. Both classes of neuron are highly direction-selective in the midranges of their spatiotemporal tuning curves, i.e., the firing rates increase during motion in the preferred direction (temporonasal movement through the visual field of the contralateral eye) and decrease during motion in the opposite direction. At high temporal and low spatial frequencies, however, the slow neurons are inhibited by motion in both directions along their preferred axis. It is argued that this bidirectional inhibition at high speeds may act to inhibit ocular following during saccades and may act as a gain control mechanism preventing excessive overshoot in eye velocity at motion onset, when retinal-slip velocities are high. 4. The fast neurons probably have two functions. First, they are suited to initiating ocular following responses when image motion is quite fast. Second, their spatiotemporal tuning makes them candidates for supplying a velocity error signal into the velocity storage mechanism, which is most prominent at high stimulus speeds. 5. Fourier analysis of the peristimulus time histograms derived from the responses of both the slow and fast neurons revealed that the main frequency components of the responses occurred at the fundamental and second harmonic frequencies of the input signal at low stimulus temporal frequencies (<3.04 Hz). At higher stimulus frequencies, the responses contained significant frequency components at higher odd-harmonics of the input signal. The change in the characteristics of the frequency components of the responses suggests that the input signal is distorted at high stimu- lus temporal frequencies such that the light and dark phases of the stimulus are not treated equally. The frequency components of the responses are discussed in the context of the motion computations underlying the responses of the NOT-DTN neurons. 6. Analysis of the receptive field properties of the neurons revealed that the fast cells probably summate the outputs of many precursor neurons that have considerably smaller receptive fields with excitatory centres and inhibitory surrounds. The same analysis shows that the slow neurons probably also receive their input from many cells with small receptive fields but in this case the precursor neurons probably have uniform excitatory receptive fields. 7. Of the neurons tested, 70% elicited a directional response when the ipsilateral eye was stimulated, the excitatory response being induced by nasotemporal motion for that eye (i.e., by the same stimulus in the visual field that is optimal for the contralateral eye). 8. In summary, the study has isolated two quite distinct types of direction- selective neurons in the NOT-DTN of the wallaby, both of which probably play an important role in controlling the slow phases of horizontal optokinetic eye movements.