Question of Reference Frames: Visual Direction-Selective Neurons in the Accessory Optic System of Goldfish

Abstract

We investigated if visual direction-selective neurons in the pretectal area (APT) of goldfish (Carassius auratus auratus) preferred visual stimuli resulting from rotations around axes corresponding to the best responsive axes of the semicircular canals [optic flow that is consistent to a maximal activation of the horizontal canal pair (yaw), to a maximal activation of the right anterior/left posterior semicircular canal pair (RALP), and to a maximal activation of the left anterior/right posterior semicircular canal pair (LARP)]. Our sample of neurons recorded in the left pretectum had two preferred axes of rotation: first, rotation around the yaw axis and second, rotation around the RALP axis. Both axes of rotation correspond to best responsive axes of the semicircular canals. For this reason, coding in a reference frame defined by the vestibular system or the pulling direction of the eye muscles is suggested. In our population of recorded APT neurons, we did not find segregation of different preferred axes of rotation into different anatomical structures. Furthermore in all axes no bias for clockwise or counterclockwise rotations was obvious. This is particularly noteworthy for the yaw axis because preference for temporo-nasal and naso-temporal rotations was found at the same recording side. Hence we conclude that in fish the accessory optic system may consist of one nucleus on each side of the midbrain only, the APT. Segregation into different nuclei coding for different axes and different senses of rotation probably first developed in amphibians.