Activity in early visual areas predicts interindividual differences in binocular rivalry dynamics

Sustained gamma band synchronization in early visual areas reflects the level of selective attention

Primate visual systems process natural images in a hierarchical manner: at the early stage, neurons are tuned to local image features, while neurons in high-level areas are tuned to abstract object categories. Standard models of visual processing assume that the transition of tuning from image features to object categories emerges gradually along the visual hierarchy. Direct tests of such models remain difficult due to confounding alteration in low-level image properties when contrasting distinct object categories. When such contrast is performed in a classic functional localizer method, the desired activation in high-level visual areas is typically accompanied with activation in early visual areas. Here we used a novel image-modulation method called SWIFT (semantic wavelet-induced frequency-tagging), a variant of frequency-tagging techniques. Natural images modulated by SWIFT reveal object semantics periodically while keeping low-level properties constant. Using functional magnetic resonance imaging (fMRI), we indeed found that faces and scenes modulated with SWIFT periodically activated the prototypical category-selective areas while they elicited sustained and constant responses in early visual areas. SWIFT and the localizer were selective and specific to a similar extent in activating category-selective areas. Only SWIFT progressively activated the visual pathway from low- to high-level areas, consistent with predictions from standard hierarchical models. We confirmed these results with criterion-free methods, generalizing the validity of our approach and show that it is possible to dissociate neural activation in early and category-selective areas. Our results provide direct evidence for the hierarchical nature of the representation of visual objects along the visual stream and open up future applications of frequency-tagging methods in fMRI.

This chapter reviews the functional anatomical bases of visual perception in the retina, the lateral geniculate nucleus (LGN) in the visual thalamus, the primary visual cortex (area V1, also called the striate cortex, and Brodmann area 17), and the extrastriate visual cortical areas of the dorsal and ventral pathways. The sections dedicated to the retina and LGN review the basic anatomical and laminar organization of these two areas, as well as their retinotopic organization and receptive field structure. We also describe the anatomical and functional differ- ences among the magnocellular, parvocelullar and koniocellular pathways. The section dedicated to area V1 reviews the functional maps in this area (retino- topic map, ocular dominance map, orientation selectivity map), as well as their anatomical relationship to each other. Special attention is given to the modular columnar organization of area V1, and to the various receptive field classes in V1 neurons. The section dedicated to extrastriate cortical visual areas describes the "where" and "what" pathways in the dorsal and ventral visual streams, and their respective physiological functions. The temporal dynamics of neurons throughout the visual pathway are critical to understanding visibility and neural information processing. We discuss the role of lateral inhibition circuits in processing spatiotemporal edges, corners, and in the temporal dynamics of vision. We also discuss the effects of eye movements on visual physiology and percep- tion in early visual areas. Our visual and oculomotor systems must achieve a very delicate balance: insufficient eye movements lead to adaptation and visual fading, whereas excessive motion of the eyes produces blurring and unstable vision during fixation. These issues are very important for neural prosthetics, in which electrodes are stabilized on the substrate.

During real-world scene perception, viewers actively direct their attention through a scene in a controlled sequence of eye fixations. During each fixation, local scene properties are attended, analyzed, and interpreted. What is the relationship between fixated scene properties and neural activity in the visual cortex? Participants inspected photographs of real-world scenes in an MRI scanner while their eye movements were recorded. Fixation-related fMRI was used to measure activation as a function of lower- and higher-level scene properties at fixation, operationalized as edge density and meaning maps, respectively. We found that edge density at fixation was most associated with activation in early visual areas, whereas semantic content at fixation was most associated with activation along the ventral visual stream including core object and scene-selective areas (lateral occipital complex, parahippocampal place area, occipital place area, and retrosplenial cortex). The observed activation from semantic content was not accounted for by differences in edge density. The results are consistent with active vision models in which fixation gates detailed visual analysis for fixated scene regions, and this gating influences both lower and higher levels of scene analysis.

March 01 2000 Neural Activity in Early Visual Areas During Global and Local Processing: A Reply to Fink, Marshall, Halligan, and Dolan In Special Collection: CogNet G. R. Mangun, G. R. Mangun Duke University Search for other works by this author on: This Site Google Scholar H. J. Heinze, H. J. Heinze Otto von Guericke University Search for other works by this author on: This Site Google Scholar M. Scholz, M. Scholz Otto von Guericke University Search for other works by this author on: This Site Google Scholar H. Hinrichs H. Hinrichs Otto von Guericke University Search for other works by this author on: This Site Google Scholar Author and Article Information G. R. Mangun Duke University H. J. Heinze Otto von Guericke University M. Scholz Otto von Guericke University H. Hinrichs Otto von Guericke University Reprint requests should be sent to: Center for Cognitive neuroscience, Box 90999, Duke University, Durham, North Carolina, 27708, USA. Online Issn: 1530-8898 Print Issn: 0898-929X © 2000 Massachusetts Institute of Technology2000 Journal of Cognitive Neuroscience (2000) 12 (2): 357–359. https://doi.org/10.1162/089892900562048 Cite Icon Cite Permissions Share Icon Share Facebook Twitter LinkedIn MailTo Views Icon Views Article contents Figures & tables Video Audio Supplementary Data Peer Review Search Site Citation G. R. Mangun, H. J. Heinze, M. Scholz, H. Hinrichs; Neural Activity in Early Visual Areas During Global and Local Processing: A Reply to Fink, Marshall, Halligan, and Dolan. J Cogn Neurosci 2000; 12 (2): 357–359. doi: https://doi.org/10.1162/089892900562048 Download citation file: Ris (Zotero) Reference Manager EasyBib Bookends Mendeley Papers EndNote RefWorks BibTex toolbar search Search Dropdown Menu toolbar search search input Search input auto suggest filter your search All ContentAll JournalsJournal of Cognitive Neuroscience Search Advanced Search This content is only available as a PDF. © 2000 Massachusetts Institute of Technology2000 Article PDF first page preview Close Modal You do not currently have access to this content.

We measured neural responses to local and global aspects of form and motion stimuli using frequency-tagged, steady-state visual evoked potentials (SSVEPs) combined with magnetic resonance imaging (MRI) data. Random dot stimuli were used to portray either dynamic Glass patterns (Glass, 1969) or coherent motion displays. SSVEPs were used to estimate neural activity in a set of fMRI-defined visual areas in each subject. To compare activity associated with local versus global processing, we analyzed two frequency components of the SSVEP in each visual area: the high temporal frequency at which the local dots were updated (30 Hz) and the much lower frequency corresponding to updates in the global structure (0.83 Hz). Local and global responses were evaluated in the context of two different behavioral tasks--subjects had to either direct their attention toward or away from the global coherence of the stimuli. The data show that the effect of attention on global and local responses is both stimulus and visual area dependent. When attention was directed away from stimulus coherence, both local and global responses were higher in the coherent motion than Glass pattern condition. Directing attention to coherence in Glass patterns enhanced global activity in areas LOC, hMT+, V4, V3a, and V1, while attention to global motion modulated responses by a smaller amount in a smaller set of areas: V4, hMT+, and LOC. In contrast, directing attention towards stimulus coherence weakly increased local responses to both coherent motion and Glass patterns. These results suggest that visual attention differentially modulates the activity of early visual areas at both local and global levels of structural encoding.

Intro: The primary agent of inhibitory neurotransmission in visual cortex, GABA, has been linked to autism etiology in animal, genetic, and post-mortem studies. Specifically, GABA is thought to be down-regulated in the autistic brain, producing an overabundance of excitatory neurotransmission. Yet, perturbations in GABAergic signaling have never been experimentally associated with behavioral symptoms in people with autism. We recently demonstrated a striking autistic deficit in binocular rivalry (Robertson et al., 2013), a visual behavior that is governed by Excitatory/Inhibitory dynamics in the brain. Here, we tested whether the dynamics of binocular rivalry in typical adults are correlated with levels of excitatory (glutamate) and inhibitory (GABA) neurotransmitters measured in vivo. Methods: We measured binocular rivalry dynamics in 18 control participants, as well as the concentration of excitatory (glutamate) and inhibitory (GABA) neurotransmitters in the primary visual (test) and motor (control) areas of each individual’s brain using Magnetic Resonance Spectroscopy (MRS). Results: GABA in V1 strongly predicted the dynamics of binocular rivalry in control individuals (Proportion of mixed percepts: rho = -0.61, p < 0.008) – where less GABA predicted slower binocular rivalry dynamics with longer mixed percepts, corresponding to the atypical dynamics we previously observed in ASD. This relationship was observed for rivalry using both simple (gratings) and complex stimuli (objects) (both r < -0.6, p < 0.009). Further, these results were specific to visual cortex: while GABA concentration in M1 predicted performance on a Go/No-Go motor task (rho = 0.67, p < 0.002), it did not predict rivalry dynamics (rho = -0.35,p > 0.19). Conclusions: Here, we demonstrate that a robust behavioral alteration in individuals with ASD strongly predicts GABA concentration measured in controls. This research may lead to the first experimental demonstration of a link between a robust autistic symptom and a prominent theory of autistic neural circuitry. Meeting abstract presented at VSS 2015

Temporal frequency and contrast tagging bias the type of competition in interocular switch rivalry

The nature of competition underlying perceptual alternations in binocular rivalry remains controversial. Interocular swapping of rivalrous stimuli can result in either slow irregular perceptual alternations that bridge multiple interocular switches or fast regular alternations that are time locked to the stimulus exchanges. We labeled either the inputs to the eyes or the individual rivalrous stimuli using temporal frequency and contrast tagging. Tagging of eye-of-origin signals enhanced the fast regular perceptual alternations associated with eye rivalry, while stimulus tagging shifted perception towards slow irregular alternations characteristic of stimulus rivalry. Thus, the type of competition in binocular rivalry can be biased based on additional cues in the visual inputs. The results are consistent with a model in which the brain combines information across multiple visual features to resolve ambiguities in visual inputs.

In this research binocular rivalry is used as a tool to investigate different aspects of visual and multisensory perception. Several experiments presented here demonstrated that touch specifically interacts with vision during binocular rivalry and that the interaction likely occurs at early stages of visual processing, probably V1 or V2. Another line of research also presented here demonstrated that human adult visual cortex retains an unexpected high degree of experience-dependent plasticity by showing that a brief period of monocular deprivation produced important perceptual consequences on the dynamics of binocular rivalry, reflecting a homeostatic plasticity. In summary, this work shows that binocular rivalry is a powerful tool to investigate different aspects of visual perception and can be used to reveal unexpected properties of early visual cortex.

Recent studies suggest that attention is necessary for perceptual alternations in binocular rivalry. It has been shown that attention plays a role in not only accelerating but also even enabling perceptual fluctuation in ongoing phase of binocular rivalry. In this study, we tested whether attention also plays a role in suppressing a rival stimulus in its initial phases by measuring proportions of mixed dominance. We hypothesized that when attention is directed toward the location of rival stimuli prior to their presentation, the proportion of mixed dominance is lower than when attention is directed away from that location because of attentional facilitation. However, we found that the proportion of mixed dominance did not differ depending on the locus of attention, although we adopted well-established experimental paradigms for manipulating spatial attention. This result suggests that attention is not a determining factor in establishing initial perceptual dominance in binocular rivalry.

BOLD activation on the groundside of figures: More suppression of grounds that competed more for figural status.

Binocular rivalry has become an important index of visual performance, both to measure ocular dominance or its plasticity, and to index bistable perception. We investigated its interindividual variability across 50 normal adults and found that the duration of dominance phases in rivalry is linked with the duration of dominance phases in another bistable phenomenon (structure from motion). Surprisingly, it also correlates with the strength of center–surround interactions (indexed by the tilt illusion), suggesting a common mechanism supporting both competitive interactions: center–surround and rivalry.In a subset of 34 participants, we further investigated the variability of short-term ocular dominance plasticity, measured with binocular rivalry before and after 2 hours of monocular deprivation. We found that ocular dominance shifts in favor of the deprived eye and that a large portion of ocular dominance variability after deprivation can be predicted from the dynamics of binocular rivalry before deprivation. The single best predictor is the proportion of mixed percepts (phases without dominance of either eye) before deprivation, which is positively related to ocular dominance unbalance after deprivation. Another predictor is the duration of dominance phases, which interacts with mixed percepts to explain nearly 50% of variance in ocular dominance unbalance after deprivation. A similar predictive power is achieved by substituting binocular rivalry dominance phase durations with tilt illusion magnitude, or structure from motion phase durations. Thus, we speculate that ocular dominance plasticity is modulated by two types of signals, estimated from psychophysical performance before deprivation, namely, interocular inhibition (promoting binocular fusion, hence mixed percepts) and inhibition for perceptual competition (promoting longer dominance phases and stronger center–surround interactions).

Binocular rivalry is perceptual alternation that occurs when different visual images are presented to each eye. Despite the intensive studies, the mechanism of binocular rivalry still remains unclear. In multistable binocular rivalry, which is a special case of binocular rivalry, it is known that the perceptual alternation between paired patterns is more frequent than that between unpaired patterns. This result suggests that perceptual transition in binocular rivalry is not a simple random process, and the memories stored in the brain can play an important role in the perceptual transition. In this study, we propose a hierarchical chaotic neural network model for multistable binocular rivalry and show that our model reproduces some characteristic features observed in multistable binocular rivalry.

The visual system employs a sophisticated balance of attentional mechanisms: salient stimuli are prioritized for visual processing, yet observers can also ignore such stimuli when their goals require directing attention elsewhere. A powerful determinant of visual salience is local feature contrast: if a local region differs from its immediate surround along one or more feature dimensions, it will appear more salient. We used high-resolution functional MRI (fMRI) at 7T to characterize the modulatory effects of bottom-up salience and top-down voluntary attention within multiple sites along the early visual pathway, including visual areas V1-V4 and the lateral geniculate nucleus (LGN). Observers viewed arrays of spatially distributed gratings, where one of the gratings immediately to the left or right of fixation differed from all other items in orientation or motion direction, making it salient. To investigate the effects of directed attention, observers were cued to attend to the grating to the left or right of fixation, which was either salient or nonsalient. Results revealed reliable additive effects of top-down attention and stimulus-driven salience throughout visual areas V1-hV4. In comparison, the LGN exhibited significant attentional enhancement but was not reliably modulated by orientation- or motion-defined salience. Our findings indicate that top-down effects of spatial attention can influence visual processing at the earliest possible site along the visual pathway, including the LGN, whereas the processing of orientation- and motion-driven salience primarily involves feature-selective interactions that take place in early cortical visual areas.NEW & NOTEWORTHY While spatial attention allows for specific, goal-driven enhancement of stimuli, salient items outside of the current focus of attention must also be prioritized. We used 7T fMRI to compare salience and spatial attentional enhancement along the early visual hierarchy. We report additive effects of attention and bottom-up salience in early visual areas, suggesting that salience enhancement is not contingent on the observer's attentional state.