Eye Movements and the Neural Basis of Context Effects on Visual Sensitivity

Abstract

The effects of context on visual sensitivity are well established (e.g., sensitivity to luminance flicker is substantially higher on mean-gray surrounds than on white or black surrounds). The neural mechanisms generating context effects, however, remain unresolved. In the absence of direct tests, some theories invoke enhancement of edges by lateral inhibition, whereas others rely on transients caused by miniature eye movements that maintain fixation. We first replicated the luminance results on human observers and found unexpectedly that sensitivity to red-green flicker is also affected by surround color, being substantially higher on mean-gray surrounds than on red or green surrounds. To identify the neural bases of both context effects, we used in vivo electrophysiological recordings of primate magnocellular and parvocellular ganglion cell responses to luminance and red-green modulations, respectively. To test neuronal sensitivity to stationary edge contrast, neuronal responses were measured at various distances from the modulation edge against various surrounds. We found no evidence of enhanced responses to stationary edges on any surrounds, ruling out lateral inhibition-type explanations. To simulate the effects of eye movements, target patches were abruptly displaced while measuring responses. Abruptly displaced edges evoked vigorous transient responses that were selective for modulation-phase on mean-gray surrounds, but were phase-invariant on other surrounds. Eye movements could thus enhance detection of flicker on mean-gray surrounds, and neurometric analyses supported a primary role for eye movements in enhancing sensitivity. In addition, the transformation of spatial edges to transient neuronal responses by eye movements provides the signals for detecting luminance and color edges in natural scenes.

A physiological perspective on fixational eye movements

“…In the absence of head and body movements, they can counteract fading of low-contrast images in the periphery (Martinez-Conde et al, 2006). Recent evidence also indicates that abrupt, saccade-like motions of a border are perceptually more important and physiologically more effective than static lateral interactions in the absence of eye movements (Ennis et al, 2014). However, the possible contributions of slower, drift-like motions were not tested.…”

The unsteady eye: an information-processing stage, not a bug

“…However, these pioneering experiments also suffered from a number of technological and methodological limitations, which cast serious doubts on extrapolating their conclusions to more natural viewing conditions [17, 21, 22]. Furthermore, the proposal of an involvement of fixational eye movements in spatial perception has recently found new support from multiples sources, including neurophysiological [16, 23, 24] and behavioral investigations [22, 25, 26], statistical examinations of retinal input signals [27, 28], and theoretical analyses of the impact of a continually moving retinal input on neural responses [15, 17, 18, 29, 30]. …”

Interaction between contours and eye movements in the perception of afterimages: A test of the signal ambiguity theory

“…This means that the retinal position of the contour, and the extent to which it was aligned with the afterimage, was less accurate in the saccade than in the fixation condition, which would explain the finding. Further, the visual system would expect sharp transients following an eye movement to a new object (Ennis et al, 2014), and afterimage perception may be further hampered if this transient is not aligned with the edges of the afterimage. The importance of contour alignment with the afterimage to produce the contour effect was confirmed in a second pilot experiment, in which we used individual eye movement data from the saccade condition in the first pilot to simulate in the fixation condition the degree of contour misalignment that occurred in the saccade condition.…”

“…Further, pilot studies revealed that the contour effect is reduced in the saccade condition relative to the fixation condition if the degree of contour alignment is not equated between the conditions. A possible reason for this is that the visual system expects sharp transients following eye movements (Ennis et al, 2014) and these would not occur for an afterimage on its own. When the contour and the afterimage are perfectly aligned (i.e., contour is gaze-contingent), sharp transients will be produced by the composite contour-afterimage signals.…”

“…The contextual influence could be a low-level effect of shared receptive field properties for contours and color in V1 (see Powell et al, 2012 for discussion). On patterned backgrounds, the edge-related activity associated with eye movements (Ennis et al, 2014) may shift the response range of neurons so that the afterimages are more difficult to distinguish from the background. On homogeneous backgrounds, where contextual changes and local edge-related activity are absent, eye movements may affect after images because perception can be biased towards the hue of the postsaccadic location (usually the background gray) via trans-saccadic integration mechanisms (Melcher, 2007; also see Powell et al, 2015 for a full discussion).…”