Representation of the stationary visual environment in the anterior thalamus of the leopard frog

Abstract

The optic tectum of the leopard frog has long been known to process visual information about prey and looming threats, stimuli characterized by their movement in the visual field. However, atectal frogs can still respond to the stationary visual environment, which therefore constitutes a separate visual subsystem in the frog. The present work seeks to characterize the stationary visual environment module in the leopard frog, beginning with the hypothesis that this module is located in the anterior thalamus, among two retinorecipient neuropil regions known as neuropil of Bellonci (NB) and corpus geniculatum (CG). First, the puzzle of how a stationary frog can see the stationary environment, in the absence of the eye movements necessary for persistence of vision, is resolved, as we show that whole-head movements caused by the frog's respiratory cycles keep the retinal image in motion. Next, the stationary visual environment system is evaluated along behavioral, anatomic, and physiological lines, and connections to other brain areas are elucidated. When the anterior thalamic visual center is disconnected, frogs show behavioral impairments in visually navigating the stationary world. Under electrophysiological probing, neurons in the NB/CG region show response properties consistent with their proposed role in processing information about the stationary visual environment: they respond to light/dark and color information, as well as reverse-engineered "stationary" stimuli (reproducing the movement on the retina of the visual backdrop caused by the frog's breathing movements), and they do not habituate. We show that there is no visuotopic map in the anterior thalamus but rather a nasal-ward constriction in the receptive fields of progressively more caudal cell groups in the NB/CG region. Furthermore, each side of the anterior thalamic visual region receives information from only the contralateral half of the visual field, as defined by the visual midline, resulting from a pattern of partial crossing over of optic nerve fibers that is also seen in the mammalian thalamic visual system, a commonality with unknown evolutionary implications. We show that the anterior thalamic visual region shares reciprocal connections with the same area on the opposite side of the brain, as well as with the posterior thalamus on both sides; there is also an anterograde ipsilateral projection from the NB/CG toward the medulla and presumably pre-motor areas.