Miriam Spering

Acting without seeing: eye movements reveal visual processing without awareness

Visual perception and eye movements are considered to be tightly linked. Diverse fields, ranging from developmental psychology to computer science, utilize eye tracking to measure visual perception. However, this prevailing view has been challenged by recent behavioral studies. Here, we review converging evidence revealing dissociations between the contents of perceptual awareness and different types of eye movement. Such dissociations reveal situations in which eye movements are sensitive to particular visual features that fail to modulate perceptual reports. We also discuss neurophysiological, neuroimaging, and clinical studies supporting the role of subcortical pathways for visual processing without awareness. Our review links awareness to perceptual-eye movement dissociations and furthers our understanding of the brain pathways underlying vision and movement with and without awareness.

Similar Effects of Feature-Based Attention on Motion Perception and Pursuit Eye Movements at Different Levels of Awareness

Feature-based attention enhances visual processing and improves perception, even for visual features that we are not aware of. Does feature-based attention also modulate motor behavior in response to visual information that does or does not reach awareness? Here we compare the effect of feature-based attention on motion perception and smooth-pursuit eye movements in response to moving dichoptic plaids—stimuli composed of two orthogonally drifting gratings, presented separately to each eye—in human observers. Monocular adaptation to one grating before the presentation of both gratings renders the adapted grating perceptually weaker than the unadapted grating and decreases the level of awareness. Feature-based attention was directed to either the adapted or the unadapted gratings motion direction or to both (neutral condition). We show that observers were better at detecting a speed change in the attended than the unattended motion direction, indicating that they had successfully attended to one grating. Speed change detection was also better when the change occurred in the unadapted than the adapted grating, indicating that the adapted grating was perceptually weaker. In neutral conditions, perception and pursuit in response to plaid motion were dissociated: While perception followed one gratings motion direction almost exclusively (component motion), the eyes tracked the average of both gratings (pattern motion). In attention conditions, perception and pursuit were shifted toward the attended component. These results suggest that attention affects perception and pursuit similarly even though only the former reflects awareness. The eyes can track an attended feature even if observers do not perceive it.

Directional Asymmetries in Human Smooth Pursuit Eye Movements

PURPOSE Humans make smooth pursuit eye movements to bring the image of a moving object onto the fovea. Although pursuit accuracy is critical to prevent motion blur, the eye often falls behind the target. Previous studies suggest that pursuit accuracy differs between motion directions. Here, we systematically assess asymmetries in smooth pursuit. METHODS In experiment 1, binocular eye movements were recorded while observers (n = 20) tracked a small spot of light moving along one of four cardinal or diagonal axes across a featureless background. We analyzed pursuit latency, acceleration, peak velocity, gain, and catch-up saccade latency, number, and amplitude. In experiment 2 (n = 22), we examined the effects of spatial location and constrained stimulus motion within the upper or lower visual field. RESULTS Pursuit was significantly faster (higher acceleration, peak velocity, and gain) and smoother (fewer and later catch-up saccades) in response to downward versus upward motion in both the upper and the lower visual fields. Pursuit was also more accurate and smoother in response to horizontal versus vertical motion. CONCLUSIONS. Our study is the first to report a consistent up-down asymmetry in human adults, regardless of visual field. Our findings suggest that pursuit asymmetries are adaptive responses to the requirements of the visual context: preferred motion directions (horizontal and downward) are more critical to our survival than nonpreferred ones.

Perceptual learning modifies untrained pursuit eye movements

Perceptual learning improves detection and discrimination of relevant visual information in mature humans, revealing sensory plasticity. Whether visual perceptual learning affects motor responses is unknown. Here we implemented a protocol that enabled us to address this question. We tested a perceptual response (motion direction estimation, in which observers overestimate motion direction away from a reference) and a motor response (voluntary smooth pursuit eye movements). Perceptual training led to greater overestimation and, remarkably, it modified untrained smooth pursuit. In contrast, pursuit training did not affect overestimation in either pursuit or perception, even though observers in both training groups were exposed to the same stimuli for the same time period. A second experiment revealed that estimation training also improved discrimination, indicating that overestimation may optimize perceptual sensitivity. Hence, active perceptual training is necessary to alter perceptual responses, and an acquired change in perception suffices to modify pursuit, a motor response.

Rapid assessment of natural visual motion integration across primate species

Our visual environment is highly dynamic and marked by continuous change. The ability to see moving objects and to interact with them is a fundamental visual skill critical for survival. Many animals rely on visual motion to capture prey or to avoid predators. In humans, visual motion perception is at the heart of daily activities such as driving a car. Since the mid-19th century, a wealth of research has helped characterize humans’ behavioral response to visual motion and elucidated the workings of the brain when viewing moving objects. Psychologists and neuroscientists have developed experimental paradigms to probe responses to visual motion, assessed with a large portfolio of techniques ranging from behavioral (psychophysical) tests, neuronal recordings, and functional magnetic resonance imaging to optogenetics. However, many of these studies used simple visual stimuli such as single dots, multiple moving dots (random dot patterns), or textures with different motion components (e.g., sine-wave gratings, Gabor patterns, and plaids). Without doubt, such synthetic stimuli are powerful in terms of affording experimenter control and limiting observed behavior to the dimension under study. However, they do not capture the dynamics and richness of our visual environment. The PNAS paper by Knoll et al. (1) introduces a highly original paradigm that allows us to assess spatiotemporal integration of visual motion information using eye movements, a continuous natural response. The authors tested three primate species (humans, macaques, and marmosets), who viewed a large display of continuously moving dots, forming an optic flow field that occupied most of the observers’ visual field. These dots moved toward or away from one point in the field [termed the focus of expansion (FOE)]. Dot velocity increased with distance from the FOE. Even though the dot field is a reduced and simplified version of what we experience … [↵][1]1To whom correspondence should be addressed. Email: mspering{at}mail.ubc.ca. [1]: #xref-corresp-1-1

The function and failure of sensory predictions

Humans and other primates are equipped with neural mechanisms that allow them to automatically make predictions about future events, facilitating processing of expected sensations and actions. Prediction‐driven control and monitoring of perceptual and motor acts are vital to normal cognitive functioning. This review provides an overview of corollary discharge mechanisms involved in predictions across sensory modalities and discusses consequences of predictive coding for cognition and behavior. Converging evidence now links impairments in corollary discharge mechanisms to neuropsychiatric symptoms such as hallucinations and delusions. We review studies supporting a prediction‐failure hypothesis of perceptual and cognitive disturbances. We also outline neural correlates underlying prediction function and failure, highlighting similarities across the visual, auditory, and somatosensory systems. In linking basic psychophysical and psychophysiological evidence of visual, auditory, and somatosensory prediction failures to neuropsychiatric symptoms, our review furthers our understanding of disease mechanisms.