Although the optic tectum in non-mammals and its mammalian homolog, the superior colliculus, are involved in avoidance behaviors, whether and how tectal neurons respond to an object approaching on a collision course towards the animal remain unclear. Here we show by single unit recording that there exist three classes of looming-sensitive neurons in the pigeon tectal layer 13, which sends looming information to the nucleus rotundus or to the tectopontine system. The response onset time of tau cells is approximately constant whereas that for rho and eta cells depends on the square root of the diameter ⁄ velocity ratio of objects looming towards the animal, the cardioacceleration of which is also linearly related to the square root of this ratio. The receptive field of tectal cells is composed of an excitatory center and an inhibitory periphery, and this periphery does not inhibit responses to looming stimuli. These results suggest that three classes of tectal neurons are specified for detecting an object approaching on a collision course towards the animal, and that rho and eta cells may signal early warning of impending collision whereas tau cells initiate avoidance responses at a constant time before collision through the tectopontine system.
Multiple visual stimuli are common in natural scenes, yet it remains unclear how multiple stimuli interact to influence neuronal responses. We investigated this question by manipulating relative signal strengths of two stimuli moving simultaneously within the receptive fields (RFs) of neurons in the extrastriate middle temporal (MT) cortex. Visual stimuli were overlapping random-dot patterns moving in two directions separated by 90°. We first varied the motion coherence of each random-dot pattern and characterized, across the direction tuning curve, the relationship between neuronal responses elicited by bidirectional stimuli and by the constituent motion components. The tuning curve for bidirectional stimuli showed response normalization and can be accounted for by a weighted sum of the responses to the motion components. Allowing nonlinear, multiplicative interaction between the two component responses significantly improved the data fit for some neurons, and the interaction mainly had a suppressive effect on the neuronal response. The weighting of the component responses was not fixed but dependent on relative signal strengths. When two stimulus components moved at different coherence levels, the response weight for the higher-coherence component was significantly greater than that for the lower-coherence component. We also varied relative luminance levels of two coherently moving stimuli and found that MT response weight for the higher-luminance component was also greater. These results suggest that competition between multiple stimuli within a neuron's RF depends on relative signal strengths of the stimuli and that multiplicative nonlinearity may play an important role in shaping the response tuning for multiple stimuli.
Misinterpretations of visual information received by the retina are called visual illusions, which are known to occur in higher brain areas. However, whether they would be also processed in lower brain structures remains unknown, and how to explain the neuronal mechanisms underlying the motion after-effect is intensely debated. We show by extracellular recording that all motion-sensitive neurons in the pigeon's pretectum respond similarly to real and illusory contours, and their preferred directions are identical for both contours in unidirectional cells, whereas these directions are changed by 90 deg for real versus illusory contours in bidirectional cells. On the other hand, some pretectal neurons produce inhibitory (excitatory) after-responses to cessation of prolonged motion in the preferred (null) directions, whose time course is similar to that of the motion after-effect reported by humans. Because excitatory and inhibitory receptive fields of a pretectal cell overlap in visual space and possess opposite directionalities, after-responses to cessation of prolonged motion in one direction may create illusory motion in the opposite direction. It appears that illusory contours and motion could be detected at the earliest stage of central information processing and processed in bottom-up streams, and that the motion after-effect may result from functional interactions of excitatory and inhibitory receptive fields with opposite directionalities.
The thalamofugal and tectofugal pathways in birds are two parallel visual pathways to the telencephalon and might be comparable to the geniculocortical and colliculo-pulvinar-cortical pathways in mammals, respectively. It is known that some tectal neurons in the tectofugal pathway can signal the time-to-collision of an approaching object. Here we show by single cell recording in the pigeon that a population of visual neurons in the nucleus opticus principalis thalami (nOPT) in the thalamofugal pathway is able to detect the distance-to-collision of a large surface approaching towards the animal. These neurons began response firing when the surface reached a threshold distance to the viewing eye and thereafter their firing rates increased exponentially until collision occurred at distance = zero. The response onset distance is nearly constant for a wide range of stimulus velocities and is equal to the product of velocity of approaching stimulus and response onset time of a nOPT cell. Furthermore, onset distance of looming responses in nOPT cells is close to that causing cardioacceleration in the pigeon viewing the approaching surface. It appears that nOPT and tectal neurons are dichotomized functionally to a large extent for detecting imminent dangers, and the pigeon’s ability to compute the distance-to-collision of an approaching surface may benefit avoiding large obstacles during flight.
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