Saccades and shifting receptive fields: anticipating consequences or selecting targets?

doi:10.1016/j.tics.2014.10.002

Trends in Cognitive Sciences

Volume 18, Issue 12, December 2014, Pages 621-628

https://doi.org/10.1016/j.tics.2014.10.002 Get rights and content

Highlights

•
We discuss the degree to which previous studies, both electrophysiological and psychophysical in monkeys and humans, provide unambiguous evidence for predictive remapping, or are in accordance with a convergent shift of receptive fields (RFs.)
•
We discuss the role of dynamic attentional deployments to saccadic targets and their possible relationship to convergent RF shifts in the context of perceptual stability and spatial distortions across eye movements.
•
We highlight outstanding questions and predictions for future research to foster our understanding of perisaccadic phenomena and perceptual stability.

Saccadic eye movements cause frequent and substantial displacements of the retinal image, but those displacements go unnoticed. It has been widely assumed that this perceived stability emerges from the shifting of visual receptive fields from their current, presaccadic locations to their future, postsaccadic locations in anticipation of the retinal consequences of saccades. Although evidence consistent with this anticipatory remapping has accumulated over the years, more recent work suggests an alternative view. In this opinion article, we examine the evidence of presaccadic receptive field shifts and their relationship to the perceptual changes that accompany saccades. We argue that both reflect the selection of targets for saccades rather than the anticipation of a displaced retinal image.

Section snippets

Predictive remapping in nonhuman primates

Humans and other primates constantly redirect their gaze in order to scan their environment. This behavior is necessary to overcome the lack of high acuity vision in the visual periphery, and is largely achieved via saccades (see Glossary). Saccades ultimately lead to the foveation of important visual stimuli, and thus allow the brain to process fine spatial details contained within those targets. However, saccades not only lead to fast sweeps of the retinal image (motion), but also introduce

Predictive remapping in humans

The first evidence of predictive remapping in human observers utilized an orientation adaptation technique and demonstrated a saccade dependent change in the resulting tilt after-effect (TAE) (Figure 3) [15]. The TAE is usually strongest if probed at the same retinocentric location where it was previously induced by an adapter stimulus. However, it was demonstrated that the TAE decreased gradually at the present, presaccadic location of the adaptor and simultaneously increased at the future,

Shifts of spatial attention prior to saccades

As previously mentioned (Box 2), a good deal of evidence indicates that spatial attention shifts to the saccade target prior to a saccade [18]. In one of the earlier psychophysical studies [19], human observers had to discriminate visual stimuli while simultaneously preparing and executing saccades to one of several locations. The authors found that discrimination performance was superior if the visual stimulus was presented at the location of the impending saccade, compared to performance at

Anticipatory remapping of attentional pointers

Evidence for predictive remapping has primarily been found in structures involved in the control of saccades, specifically, area LIP, the SC, and the FEF. Furthermore, LIP, the SC, and, particularly, the FEF (see Box 3) have been implicated in the control of visuospatial attention, and all three areas exhibit properties suggesting they each contain a ‘priority map’ [33], in which peaks of activity point to physically salient and/or behaviorally relevant stimuli. Recently [34], it was postulated

Concluding remarks and future directions

We have discussed the evidence of RF shifts during the preparation of saccadic eye movements. Thus far, this evidence suggests that previous observations of predictive remapping may be explained instead by a convergence of RFs toward the targets of saccades. The apparent convergence of RFs seems to be in accordance with other neurophysiological and psychophysical evidence of a predominant role of saccadic targets in vision 46, 47, 48, 49, 50, 51, 52. However, future experiments will be

Acknowledgments

This work was supported by National Institutes of Health grant EY014924.

Glossary

Compression of visual space: a visual illusion occurring around the time of saccades. Briefly presented stimuli are perceptually mislocalized closer to saccade targets. This phenomenon might be related to gain modulation induced distortions of neuronal population responses.
Focus of convergence: point in retinocentric coordinates to which receptive fields shift. Here, each point of convergence may simultaneously reflect a peak in gain modulation of neuronal responses, in the probability of a

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Most research on forebrain attention networks focuses not on the mechanisms that generate selection signals, but rather on pathways that distribute selection signals and the mechanisms by which these signals regulate the quality of the selected information [4,7,60,61]. Effects on neural activity that correlate with attention include increases in neuronal sensitivity, gain, decorrelation of activity with neighboring neurons, periodic synchronization of activity both within a cortical area and across areas, and, at high levels of processing, dynamic shifts or sharpening of receptive field tuning (e.g., for location or feature values), resulting in the preferential representation of the attended stimulus [62–65]. At the same time, neuronal responses to distracting stimuli tend to be suppressed [66,67].
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Trends in Cognitive Sciences

OpinionSaccades and shifting receptive fields: anticipating consequences or selecting targets?

Highlights

Section snippets

Predictive remapping in nonhuman primates

Predictive remapping in humans

Shifts of spatial attention prior to saccades

Anticipatory remapping of attentional pointers

Concluding remarks and future directions

Acknowledgments

Glossary

Vision Res.

Curr. Opin. Neurobiol.

Trends Neurosci.

Neuron

Vision Res.

Vision Res.

Vision Res.

Neuron

Neuron

Vision Res.

Neuron

Trends Cogn. Sci.

Trends Cogn. Sci.

Vision Res.

Neuron

Vision Res.

Vision Res.

Neuropsychologia

Brain Res. Cogn. Brain Res.

Neuron

Neuron

Neuron

Brain Res.

The updating of the representation of visual space in parietal cortex by intended eye movements

Science

Neurons in the monkey superior colliculus predict the visual result of impending saccadic eye movements

J. Neurophysiol.

Spatial processing in the monkey frontal eye field. I. Predictive visual responses

J. Neurophysiol.

Influence of the thalamus on spatial visual processing in frontal cortex

Nature

Updating of the visual representation in monkey striate and extrastriate cortex during saccades

Proc. Natl. Acad. Sci. U.S.A.

Modulation of shifting receptive field activity in frontal eye field by visual salience

J. Neurophysiol.

Division of labor in frontal eye field neurons during presaccadic remapping of visual receptive fields

J. Neurophysiol.

Anticipatory remapping of attentional priority across the entire visual field

J. Neurosci.

Visual space is compressed in prefrontal cortex before eye movements

Nature

Predictive remapping of visual features precedes saccadic eye movements

Nat. Neurosci.

Visual stability and the motion aftereffect: a psychophysical study revealing spatial updating

PLoS ONE

Anticipatory saccade target processing and the presaccadic transfer of visual features

J. Neurosci.

The role of attention in saccadic eye movements

Percept. Psychophys.

Attention to both space and feature modulates neuronal responses in macaque area V4

J. Neurophysiol.

Enhanced activation of neurons in prelunate cortex before visually guided saccades of trained rhesus monkeys

Exp. Brain Res.

Parallel and serial neural mechanisms for visual search in macaque area V4

Science

Opinion
Saccades and shifting receptive fields: anticipating consequences or selecting targets?