Journal Article

Tectal microcircuit generating visual selection commands on gaze-controlling neurons

Saitoh, Kazuya, Kardamakis, Andreas A., Grillner, Sten

2015

Overview

The optic tectum (called superior colliculus in mammals) is critical for eye–head gaze shifts as we navigate in the terrain and need to adapt our movements to the visual scene. The neuronal mechanisms underlying the tectal contribution to stimulus selection and gaze reorientation remains, however, unclear at the microcircuit level. To analyze this complex—yet phylogenetically conserved—sensorimotor system, we developed a novel in vitro preparation in the lamprey that maintains the eye and midbrain intact and allows for whole-cell recordings from prelabeled tectal gaze-controlling cells in the deep layer, while visual stimuli are delivered. We found that receptive field activation of these cells provide monosynaptic retinal excitation followed by local GABAergic inhibition (feedforward). The entire remaining retina, on the other hand, elicits only inhibition (surround inhibition). If two stimuli are delivered simultaneously, one inside and one outside the receptive field, the former excitatory response is suppressed. When local inhibition is pharmacologically blocked, the suppression induced by competing stimuli is canceled. We suggest that this rivalry between visual areas across the tectal map is triggered through long-range inhibitory tectal connections. Selection commands conveyed via gaze-controlling neurons in the optic tectum are, thus, formed through synaptic integration of local retinotopic excitation and global tectal inhibition. We anticipate that this mechanism not only exists in lamprey but is also conserved throughout vertebrate evolution. Significance Neurons in the optic tectum are involved in stimulus selection and also control gaze reorientation. This study relies on an in vitro preparation that allows visual activation of the retina while providing accessibility for whole-cell recordings from specific cells that control gaze action. We show the tectal (collicular in mammals) GABAergic interneurons generate rivalry between visual areas and that tectal gaze-controlling cells integrate this inhibition along with local retinal excitation to form stimulus selection commands that will move the eyes and head, and may also contribute to edge detection. We propose that this subcortical visuomotor circuit is phylogenetically conserved throughout vertebrate evolution.

• Publisher: National Academy of Sciences,National Acad Sciences
• Subject: Algorithms / Animals / Biological Sciences / Brain / Cells / Eye / GABAergic Neurons - cytology / GABAergic Neurons - metabolism / GABAergic Neurons - physiology / gamma-Aminobutyric Acid - metabolism / head / Immunohistochemistry / interneurons / Interneurons - cytology / Interneurons - metabolism / Interneurons - physiology / Lampreys - anatomy & histology / Lampreys - metabolism / Lampreys - physiology / mammals / Microscopy, Confocal / Microscopy, Fluorescence / Models, Neurological / Neural Inhibition - physiology / Neurons / Patch-Clamp Techniques / Petromyzontidae / Phylogenetics / phylogeny / PNAS Plus / Retina / Retinaldehyde - physiology / Superior Colliculi - cytology / Superior Colliculi - metabolism / Superior Colliculi - physiology / Synapses - physiology / Synaptic Transmission - physiology / Visual Pathways - cytology / Visual Pathways - metabolism / Visual Pathways - physiology