We use multidisciplinary approaches to study neuronal properties and circuits underlying visual information processing, including eye movements, visual motion perception, the formation and modulation of receptive fields, and centrifugal modulation of vision.
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Neuronal circuits controlling eye movements and saccadic suppression.
Our eyes move frequently to fixate a target of interest or stabilize the visual world. We found that a saccade in the pigeon causes inhibition followed by enhancement of firing activity in the telencephalon, thalamus and pretectal nucleus (nLM), and opposite responses in the accessory optic nucleus (nBOR). Saccadic responses in telencephalic neurons originate from thalamic cells, whose saccadic responses in turn originate from nLM and nBOR, both of which are involved in optokinetic nystagmus. Saccade-related omnipause neurons in the brainstem raphe complex inhibit nBOR and excite nLM, and thus produce saccadic responses in optokinetic neurons. It appears that saccadic responses in telencephalic neurons are generated by corollary discharge signals from brainstem neurons via optokinetic and thalamic neurons. These corollary signals make the visual world clear and stable during saccades.
Horizontal eye movements are actuated by extraocular muscles innervated by the abducens and oculomotor nuclei. We found that there exist three types of abducens neurons in terms of firing patterns corresponding to a shift and oscillations of a saccade. Shift-related neurons discharge sustained firing around the shift, oscillation-related neurons produce bursts accompanying oscillations, and saccade-related neurons discharge both sustained firing and bursts peri-saccadically. The latter two types are divided each into two groups: burst activity begins before (leading) or after (lagging) the onset of nasotemporal saccades. The lagging group neurons project to the contralateral oculomotor nucleus. The optokinetic nuclei nLM /nBOR and raphe complex send differential signals to abducens neurons to generate three types of firing patterns, and thereby initiate shift and oscillation components of a horizontal saccade.
- Visual motion detection and illusion.
Detecting visual motion is vital for avoiding dangerous objects / surfaces or intercepting desirable targets. Physically, motion is described by its acceleration, speed, and direction. We found that a group of pretectal neurons is characterized by plateau-shaped speed tuning curves in which firing rate is identical over a wide range of speeds, allowing these neurons to encode unambiguously the change rate of speed over time, i.e. acceleration of stimulus motion. Several similarities between visual and vestibular systems suggest that both share temporal reference frame, and multimodal integration helps in detecting self-motion of an organism.
Three classes of neurons in tectal layer 13 can compute the time-to-collision of an object approaching towards the viewing eye. Comparisons between the response onset time of tectal neurons and that of cardioacceleration in the pigeon shows 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. On the other hand, a group of thalamic neurons is able to compute the distance-to-collision of an approaching large surface, and the response onset distance in a neuron equals to the product of approaching stimulus speed and the response onset time in the neuron. It appears that tectofugal and thalamofugal pathways are dichotomized functionally to a large extent for detecting imminent dangers.
Visual motion or an object we see does not always exist in the real world due to misinterpretations of retinal images by the brain. Elucidation of such visual illusions would bridge neuronal activity and psychology. We found that a group of 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 aftereffect reported by observers. Because excitatory (ERF) and inhibitory (IRF) receptive fields of a pretectal cell possess opposite directionalities, after-responses in one direction may create illusory motion in the opposite direction. It appears that the motion aftereffect or waterfall illusion may result from functional interactions of ERF and IRF with opposite directionalities.
- Formation and modulation of receptive fields.
The receptive field is one of the most important concepts in visual neuroscience, and thus its properties, formation and modulation have been extensively studied. We found that the magnocellular (Imc) and parvocellular (Ipc) divisions of the nucleus isthmi in the pigeon midbrain are visual centers and exert excitatory and inhibitory actions on tectal cells, respectively. The Imc-tectal pathway is mediated by glutamate via AMPA / NMDA receptors and acetylcholine via muscarinic receptors, whereas the Ipc-tectal pathway is mediated by GABA and GABAA receptors. Further, Imc and Ipc differentially modulate ERF and IRF of tectal neurons, respectively. These two pathways may work together in a winner-take-all manner, so that the animal could attend only to one of several competing targets in the visual field.
On the other hand, we found that tectal neurons with circular ERF can modulate isthmic neurons with elongated ERF. Single cell recording and inactivation experiments show that the elongated ERF of an isthmic neuron is constructed from aligned circular ERFs of tectal neurons whereas flanked IRFs originate from intranuclear inhibitory circuits. The orientation selectivity of an isthmic neuron is mainly determined by its ERF and sharply tuned by IRFs. Tectal neurons converging onto an isthmic neuron are arranged in a narrow dorsoventral column in tectum. According to the retinotectal map, their ERFs are aligned in a line orthogonal to the horizontal axis of the visual field, in agreement with computer-mapped ERF distribution.
- Centrifugal modulation of vision
Visual information is processed and transmitted from the retina to the brain and from the brain back to the retina as well. We found that tectal neurons in the pigeon directly activate neurons in the isthmo-optic nucleus (ION), which project from the midbrain to the retina, and that tectal fibers contact ION neurons in one-to-one fashion. Tecto-ION synapses use glutamate via AMPA receptors (75%) or nitric oxide (25%) as transmitters. Gap junctions and electrical field effects may play essential roles in synchronizing ION activity. Topographic modulation of tectal activity by ION neurons implies that ION may be involved in switching visual attention to the predator when it appears in the sky.