Selective postsaccadic enhancement of motion perception.
ABSTRACT: Saccadic eye movements can drastically affect motion perception: during saccades, the stationary surround is swept rapidly across the retina and contrast sensitivity is suppressed. However, after saccades, contrast sensitivity is enhanced for color and high-spatial frequency stimuli and reflexive tracking movements known as ocular following responses (OFR) are enhanced in response to large field motion. Additionally, OFR and postsaccadic enhancement of neural activity in primate motion processing areas are well correlated. It is not yet known how this postsaccadic enhancement arises. Therefore, we tested if the enhancement can be explained by changes in the balance of centre-surround antagonism in motion processing, where spatial summation is favoured at low contrasts and surround suppression is favoured at high contrasts. We found motion perception was selectively enhanced immediately after saccades for high spatial frequency stimuli, consistent with previously reported selective postsaccadic enhancement of contrast sensitivity for flashed high spatial frequency stimuli. The observed enhancement was also associated with changes in spatial summation and suppression, as well as contrast facilitation and inhibition, suggesting that motion processing is augmented to maximise visual perception immediately after saccades. The results highlight that spatial and contrast properties of underlying neural mechanisms for motion processing can be affected by an antecedent saccade for highly detailed stimuli and are in line with studies that show behavioural and neuronal enhancement of motion processing in non-human primates.
Project description:Most people easily learn to recognize new faces and places, and with more extensive practice they can become experts at visual tasks as complex as radiological diagnosis and action video games. Such perceptual plasticity has been thoroughly studied in the context of training paradigms that require constant fixation. In contrast, when observers learn under more natural conditions, they make frequent saccadic eye movements. Here we show that such eye movements can play an important role in visual learning. Observers performed a task in which they executed a saccade while discriminating the motion of a cued visual stimulus. Additional stimuli, presented simultaneously with the cued one, permitted an assessment of the perceptual integration of information across visual space. Consistent with previous results on perisaccadic remapping [M. Szinte, D. Jonikaitis, M. Rolfs, P. Cavanagh, H. Deubel, J. Neurophysiol. 116, 1592-1602 (2016)], most observers preferentially integrated information from locations representing the presaccadic and postsaccadic retinal positions of the cue. With extensive training on the saccade task, these observers gradually acquired the ability to perform similar motion integration without making eye movements. Importantly, the newly acquired pattern of spatial integration was determined by the metrics of the saccades made during training. These results suggest that oculomotor influences on visual processing, long thought to subserve the function of perceptual stability, also play a role in visual plasticity.
Project description:Surround suppression contributes to important functions in visual processing, such as figure-ground segregation; however, this benefit comes at the cost of decreased neuronal sensitivity. Studies of receptive fields at several levels of the visual hierarchy have demonstrated that surround suppression is reduced for low contrast stimuli, thereby improving neuronal sensitivity. We investigated whether this reduction of surround suppression reflects a general processing strategy to boost sensitivity for weak signals by summing them over a larger region of the visual field (spatial integration) or if the reduction is limited to specialized stimulus conditions. To do this, we used stochastic motion stimuli to measure surround suppression in area MT of alert macaque monkeys. While varying stimulus size we also varied the strength of two other critical stimulus features: contrast and coherence (i.e., the proportion of dots moving in the preferred direction of the neuron). We found that reducing stimulus contrast weakened surround suppression, but reducing stimulus coherence had the opposite effect, indicating that diminished surround suppression is not a universal response to stimuli of low signal-to-noise. This can be partially explained by our other finding, which is that surrounds in MT are very broadly direction tuned. Instead of producing a reduction of surround suppression that would improve the ability of the neuron to integrate preferred direction motion, low coherence stimuli activated the broadly tuned surrounds relatively better than the centers, which are generally more direction selective. Our results are consistent with a normalization mechanism of surround suppression that pools broadly across multiple stimulus dimensions.
Project description:Ocular following responses (OFRs) are the initial tracking eye movements elicited at ultra-short latency by sudden motion of a textured pattern. We wished to evaluate quantitatively the impact that subcortical stages of visual processing might have on the OFRs. In three experiments we recorded the OFRs of human subjects to brief horizontal motion of 1D vertical sine-wave gratings restricted to an elongated horizontal aperture. Gratings were composed of a variable number of abutting horizontal strips where alternate strips were in counterphase. In one of the experiments we also utilized gratings occupying a variable number of horizontal strips separated vertically by mean-luminance gaps. We modeled retinal center/surround receptive fields as a difference of two 2-D Gaussian functions. When the characteristics of such local filters were selected in accord with the known properties of primate retinal ganglion cells, a single-layer model was capable to quantitatively account for the observed changes in the OFR amplitude for stimuli composed of counterphase strips of different heights (Experiment 1), for a wide range of stimulus contrasts (Experiment 2) and spatial frequencies (Experiment 3). A similar model using oriented filters that resemble cortical simple cells was also able to account for these data. Since similar filters can be constructed from the linear summation of retinal filters, and these filters alone can explain the data, we conclude that retinal processing determines the response to these stimuli. Thus, with appropriately chosen stimuli, OFRs can be used to study visual spatial integration processes as early as in the retina.
Project description:Perception of a stable visual world despite eye motion requires integration of visual information across saccadic eye movements. To investigate how the visual system deals with localization of moving visual stimuli across saccades, we observed spatiotemporal changes of receptive fields (RFs) of motion-sensitive neurons across periods of saccades in the middle temporal (MT) and medial superior temporal (MST) areas. We found that the location of the RFs moved with shifts of eye position due to saccades, indicating that motion-sensitive neurons in both areas have retinotopic RFs across saccades. Different characteristic responses emerged when the moving visual stimulus was turned off before the saccades. For MT neurons, virtually no response was observed after the saccade, suggesting that the responses of these neurons simply reflect the reafferent visual information. In contrast, most MST neurons increased their firing rates when a saccade brought the location of the visual stimulus into their RFs, where the visual stimulus itself no longer existed. These findings suggest that the responses of such MST neurons after saccades were evoked by a memory of the stimulus that had preexisted in the postsaccadic RFs ("memory remapping"). A delayed-saccade paradigm further revealed that memory remapping in MST was linked to the saccade itself, rather than to a shift in attention. Thus, the visual motion information across saccades was integrated in spatiotopic coordinates and represented in the activity of MST neurons. This is likely to contribute to the perception of a stable visual world in the presence of eye movements.
Project description:The spatial context has strong effects on visual processing. Psychophysics and modeling studies have provided evidence that the surround context can systematically modulate the perception of center stimuli. For motion direction, these center-surround interactions are considered to come from spatio-directional interactions between direction of motion tuned neurons, which are attributed to the middle temporal (MT) area. Here, we investigated through psychophysics experiments on human subjects changes with spatial separation in center-surround inhibition and motion direction interactions. Center-surround motion repulsion effects were measured under near-and far-surround conditions. Using a simple physiological model of the repulsion effect we extracted theoretical population parameters of surround inhibition strength and tuning widths with spatial distance. All 11 subjects showed clear motion repulsion effects under the near-surround condition, while only 10 subjects showed clear motion repulsion effects under the far-surround condition. The model predicted human performance well. Surround inhibition under the near-surround condition was significantly stronger than that under the far-surround condition, and the tuning widths were smaller under the near-surround condition. These results demonstrate that spatial separation can both modulate the surround inhibition strength and surround to center tuning width.
Project description:As the neural representation of visual information is initially coded in retinotopic coordinates, eye movements (saccades) pose a major problem for visual stability. If no visual information were maintained across saccades, retinotopic representations would have to be rebuilt after each saccade. It is currently strongly debated what kind of information (if any at all) is accumulated across saccades, and when this information becomes available after a saccade. Here, we use a motion illusion to examine the accumulation of visual information across saccades. In this illusion, an annulus with a random texture slowly rotates, and is then replaced with a second texture (motion transient). With increasing rotation durations, observers consistently perceive the transient as large rotational jumps in the direction opposite to rotation direction (backward jumps). We first show that accumulated motion information is updated spatiotopically across saccades. Then, we show that this accumulated information is readily available after a saccade, immediately biasing postsaccadic perception. The current findings suggest that presaccadic information is used to facilitate postsaccadic perception and are in support of a forward model of transsaccadic perception, aiming at anticipating the consequences of eye movements and operating within the narrow perisaccadic time window.
Project description:As stimulus size increases, motion direction of high-contrast patterns becomes increasingly harder to perceive. This counterintuitive behavioral result, termed "spatial suppression," is hypothesized to reflect center-surround antagonism-a receptive field property ubiquitous in sensory systems. Prior research proposed that spatial suppression of motion signals is a direct correlate of center-surround antagonism within cortical area MT. Here, we investigated whether human MT/V5 is indeed causally involved in spatial suppression of motion signals. The key assumption is that a disruption of neural mechanisms that play a critical role in spatial suppression could allow these normally suppressed motion signals to reach perceptual awareness. Thus, our hypothesis was that a disruption of MT/V5 should weaken spatial suppression and, consequently, improve motion perception of large, moving patterns. To disrupt MT/V5, we used offline 1 Hz transcranial magnetic stimulation (TMS)-a method that temporarily attenuates normal functioning of the targeted cortex. Early visual areas were also targeted as a control site. The results supported our hypotheses and showed that disruption of MT/V5 improved motion discrimination of large, moving stimuli, presumably by weakening surround suppression strength. This effect was specific to MT/V5 stimulation and contralaterally presented stimuli. Evidently, the critical neural constraints limiting motion perception of large, high-contrast stimuli involve MT/V5. Additionally, our findings mimic spatial suppression deficits that are observed in several patient populations and implicate impaired MT/V5 processes as likely neural correlates for the reported perceptual abnormalities in the elderly, patients with schizophrenia and those with a history of depression.
Project description:Humans are able to integrate pre- and postsaccadic percepts of an object across saccades to maintain perceptual stability. Previous studies have used Maximum Likelihood Estimation (MLE) to determine that integration occurs in a near-optimal manner. Here, we compared three different models to investigate the mechanism of integration in more detail: an early noise model, where noise is added to the pre- and postsaccadic signals before integration occurs; a late-noise model, where noise is added to the integrated signal after integration occurs; and a temporal summation model, where integration benefits arise from the longer transsaccadic presentation duration compared to pre- and postsaccadic presentation only. We also measured spatiotemporal aspects of integration to determine whether integration can occur for very brief stimulus durations, across two hemifields, and in spatiotopic and retinotopic coordinates. Pre-, post-, and transsaccadic performance was measured at different stimulus presentation durations, both at the saccade target and a location where the pre- and postsaccadic stimuli were presented in different hemifields across the saccade. Results showed that for both within- and between-hemifields conditions, integration could occur when pre- and postsaccadic stimuli were presented only briefly, and that the pattern of integration followed an early noise model. Whereas integration occurred when the pre- and post-saccadic stimuli were presented in the same spatiotopic coordinates, there was no integration when they were presented in the same retinotopic coordinates. This contrast suggests that transsaccadic integration is limited by early, independent, sensory noise acting separately on pre- and postsaccadic signals.
Project description:The perception of motion is considered critical for performing everyday tasks, such as locomotion and driving, and relies on different levels of visual processing. However, it is unclear whether healthy aging differentially affects motion processing at specific levels of processing, or whether performance at central and peripheral spatial eccentricities is altered to the same extent. The aim of this study was to explore the effects of aging on hierarchically different components of motion processing: the minimum displacement of dots to perceive motion (Dmin), the minimum contrast and speed to determine the direction of motion, spatial surround suppression of motion, global motion coherence (translational and radial), and biological motion. We measured motion perception in both central vision and at 15° eccentricity, comparing performance in 20 older (60-79 years) and 20 younger (19-34 years) adults. Older adults had significantly elevated thresholds, relative to younger adults, for motion contrast, speed, Dmin, and biological motion. The differences between younger and older participants were of similar magnitude in central and peripheral vision, except for surround suppression of motion, which was weaker in central vision for the older group, but stronger in the periphery. Our findings demonstrate that the effects of aging are not uniform across all motion tasks. Whereas the performance of some tasks in the periphery can be predicted from the results in central vision, the effects of age on surround suppression of motion shows markedly different characteristics between central and peripheral vision.
Project description:Major depressive disorder (MDD) is a mood disorder that is not traditionally considered to affect the visual system. However, recent findings have reported decreased cortical levels of the inhibitory neurotransmitter GABA in occipital cortex. To explore possible functional consequences of MDD on visual processing, we applied a psychophysical visual motion processing task in which healthy young adults typically exhibit impaired perceptual discrimination of large high-contrast stimuli. It has been suggested that this phenomenon, spatial suppression, is mediated by GABAergic center-surround antagonism in visual pathways. Based on previous findings linking MDD to occipital GABA dysfunction, we hypothesized that MDD patients would exhibit decreased spatial suppression, leading to the counterintuitive hypothesis of better psychophysical performance. Indeed, motion perception for typically suppressed stimuli was enhanced in patients with MDD compared with age-matched controls. Furthermore, the degree of spatial suppression correlated with an individual's illness load; patients with greater lifetime duration of depression exhibited the least spatial suppression and performed the best in the high-contrast motion discrimination task. Notably, this decrease in spatial suppression persisted beyond recovery and without the confound of acute illness or treatment; all patients had been clinically recovered and unmedicated for several months at the time of testing, suggesting that depression has ubiquitous consequences that may persist long after mood symptoms have receded. This finding raises the possibility that spatial suppression may represent a sensitive endophenotypic marker of trait vulnerability in MDD.