The Neural Basis of Dim-Light Vision in Echolocating Bats

Abstract

Echolocating bats evolved a sophisticated biosonar imaging system that allows for a life in dim-light habitats. However, especially for far-range operations such as homing, bats can support biosonar by vision. Large eyes and a retina that mainly consists of rods are assumed to be the optical adjustments that enable bats to use visual information at low light levels. In addition to optical mechanisms, many nocturnal animals evolved neural adaptations such as elongated integration times or enlarged spatial sampling areas to further increase the sensitivity of their visual system by temporal or spatial summation of visual information. The neural mechanisms that underlie the visual capabilities of echolocating bats have, however, so far not been investigated. To shed light on spatial and temporal response characteristics of visual neurons in an echolocating bat, Phyllostomus discolor, we recorded extracellular multiunit activity in the retino-recipient superficial layers of the superior colliculus (SC). We discovered that response latencies of these neurons were generally in the mammalian range, whereas neural spatial sampling areas were unusually large compared to those measured in the SC of other mammals. From this we suggest that echolocating bats likely use spatial but not temporal summation of visual input to improve visual performance under dim-light conditions. Furthermore, we hypothesize that bats compensate for the loss of visual spatial precision, which is a byproduct of spatial summation, by integration of spatial information provided by both the visual and the biosonar systems. Given that knowledge about neural adaptations to dim-light vision is mainly based on studies done in non-mammalian species, our novel data provide a valuable contribution to the field and demonstrate the suitability of echolocating bats as a nocturnal animal model to study the neurophysiological aspects of dim-light vision.