Cortical Substrates of Perceptual Stability during Eye Movements

Abstract

We are usually unaware of retinal image motion resulting from our own movement. For instance, during slow-tracking eye movements, the world around us remains perceptually stable despite the retinal image slip induced by the eye movement. This example of perceptual invariance is achieved by subtracting an internal reference signal, reflecting the eye movement, from the retinal motion signal. If the two cancel each other, visual structures, which do not move, will also be perceived as nonmoving. If, however, the reference signal is too small or too large, a false eyemovement-induced motion of the external world will be perceived. We have exploited our ability to manipulate the size of the reference signal in an attempt to reveal the structures in visual cortex, encoding the perception of self-induced visual motion rather than the retinal motion signal. Using EEG and lately also MEG recordings in human subjects and single-unit recordings in monkeys, we have been able to show that our ability to perceive the world as stationary despite eye-movement-induced retinal image slip is based on "late" parts of the cortical hierarchy of motion processing, sparing the early stages up to cortical area MT and, among others, involving cortex at the junction between the parietal and temporal lobes close to the parieto-insular-vestibular cortex. Lesions of this network in humans render the visual system unable to compensate for the visual consequences of eye movements, giving rise to severe dizziness, whenever the eyes move smoothly.

A primer on motion visual evoked potentials

“…Nevertheless, the visual world seems stable during eye movements. Thier et al [146] investigated this using the Filehne illusion. They found the first effect in the VEP around 300 ms and concluded that the distinction between both types of motion is achieved upstream from area MT from which the earlier N2 arises.…”

Keep your eyes on the ball: smooth pursuit eye movements enhance prediction of visual motion

“…Recent neurophysiological studies in monkeys showed that MT activity was mostly correlated with target motion on the retina, whereas responses of some MST neurons were correlated with target motion on the screen, i.e., relative to the head and independent of the pursuit response (Chukoskie and Movshon 2009;Inaba et al 2007). The finding that some MST neurons veridically encode retinal image motion during pursuit indicates that neurons in higher cortical visual areas compensate for eye-movement-induced motion signals during pursuit (see also Bradley et al 1996;Dicke et al 2008;Shenoy et al 1999, Thier et al 2001.…”

Corollary discharge circuits in the primate brain

“…This implies a corrective mechanism within the oculomotor networks of the brain. One model of this mechanism, based closely on the classical concepts of Efferenzkopie (“efference copy”) by von Holst and Mittelstaedt [3] and Willensanstrengung (“effort of will”) by von Helmholtz [7], postulates a cancellation process mediated at least in part by an internal reference signal [8]. This internal reference signal, generated from a CD that represents each eye movement, is a prediction of the imminent retinal image motion.…”