Neural Correlates of Spontaneous Direction Reversals in Ambiguous Apparent Visual Motion

doi:10.1006/nimg.2001.1030

NeuroImage

Volume 15, Issue 4, April 2002, Pages 908-916

https://doi.org/10.1006/nimg.2001.1030 Get rights and content

Abstract

Looking at bistable visual stimuli, the observer experiences striking transitions between two competing percepts while the physical stimulus remains the same. Using functional imaging techniques, it is therefore possible to isolate neural correlates of perceptual changes that are independent of the low-level aspects of the stimulus. Previous experiments have demonstrated distributed activations in human extrastriate visual cortex related to switches between competing percepts. Here we asked where extrastriate responses still occur with a bistable stimulus that minimizes the cognitive difference between the two percepts. We used the “spinning wheel illusion,” a bistable apparent motion stimulus of which both possible percepts correspond to the same object, share the same center, and are perceived as identically patterned stimuli moving at the same speed and changing only in direction. Using functional magnetic resonance imaging, we analyzed the spatial distribution of event-related activations occurring during spontaneous reversals of perceived direction of motion. In accordance with earlier neuroimaging findings for bistable percepts, we observed event-related activations in several frontal and parietal areas, including the superior parietal cortex bilaterally, the right inferior parietal cortex, and the premotor and inferior frontal cortex of both hemispheres. Furthermore, we found bilateral activations in the occipitotemporal junction (hMT+/V5) and in the lateral occipital sulcus (“KO”) posterior to hMT+/V5, but not in areas of the “ventral stream” of cortical visual processing. Our data suggest that, while a frontoparietal network subserves more general aspects in bistable visual perception, the activations in functionally specialized extrastriate visual cortex are highly category- or attribute-specific.

References (61)

D.M. Barch et al.
Dissociating working memory from task difficulty in human prefrontal cortex
Neuropsychologia
(1997)
J. Duncan et al.
Common regions of the human frontal lobe recruited by diverse cognitive demands
Trends Neurosci.
(2000)
R. Elliott et al.
Ventromedial prefrontal cortex mediates guessing
Neuropsychologia
(1999)
C. Frith et al.
The neural correlates of conscious experience: An experimental framework
Trends Cognit. Sci.
(1999)
T. Paus
Location and function of the human frontal eye-field: A selective review
Neuropsychologia
(1996)
G. Rees
Neuroimaging of visual awareness in patients and normal subjects
Curr. Opin. Neurobiol.
(2001)
F. Tong et al.
Binocular rivalry and visual awareness in human extrastriate cortex
Neuron.
(1998)
S.P. Ahlfors et al.
Spatiotemporal activity of a cortical network for processing visual motion revealed by MEG and fMRI
J. Neurophysiol.
(1999)
A. Borsellino et al.
Effects of visual angle on perspective reversal for ambiguous patterns
Perception
(1982)
A. Borsellino et al.
Reversal time distribution in the perception of visual ambiguous stimuli
Kybernetik
(1972)

C. Büchel et al.

The functional anatomy of attention to visual motion. A functional MRI study

Brain

(1998)

M.A. Burock et al.

Randomized event-related experimental designs allow for extremely rapid presentation rates using functional MRI

NeuroReport

(1998)

D. Chawla et al.

The physiological basis of attentional modulation in extrastriate visual areas

Nat. Neurosci.

(1999)

M. Corbetta

Frontoparietal cortical networks for directing attention and the eye to visual locations: Identical, independent, or overlapping neural systems?

Proc. Natl. Acad. Sci. USA

(1998)

M. Corbetta et al.

A PET study of visuospatial attention

J. Neurosci.

(1993)

L. Cornette et al.

Human brain regions involved in direction discrimination

J. Neurophysiol.

(1998)

S.Z. Cui et al.

Both sides of human cerebellum involved in preparation and execution of sequential movements

NeuroReport

(2000)

J. Downar et al.

A multimodal cortical network for the detection of changes in the sensory environment

Nat. Neurosci.

(2000)

C.J. Duffy et al.

Multiple temporal components of optic flow responses in MST neurons

Exp. Brain Res.

(1997)

F.H. Duffy et al.

Eye movement-related inhibition of primate visual neurons

Brain Res.

(1975)

P. Dupont et al.

The kinetic occipital region in human visual cortex

Cereb. Cortex

(1997)

D. Finlay et al.

The waggon-wheel effect

Perception

(1984)

D.J. Finlay et al.

Speed of apparent motion and the wagon-wheel effect

Percept. Psychophys.

(1987)

K.J. Friston et al.

Statistical parametric maps in functional imaging: A general linear approach

Hum. Brain Mapp.

(1995)

R. Goebel et al.

The constructive nature of vision: Direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery

Eur. J. Neurosci.

(1998)

C.L. Grady et al.

Effect of task difficulty on cerebral blood flow during perceptual matching of faces

Hum. Brain Mapp.

(1996)

D.J. Heeger et al.

Motion opponency in visual cortex

J. Neurosci.

(1999)

O. Josephs et al.

Event-related functional magnetic resonance imaging: Modelling, inference and optimization

Philos. Trans. R. Soc. London B Biol. Sci.

(1999)

O. Josephs et al.

Event-related fMRI

Hum. Brain Mapp.

(1997)

J.A.S. Kelso et al.

Multistability and metastability in perceptual and brain dynamics

Cited by (115)

Specialized late cingulo-opercular network activation elucidates the mechanisms underlying decisions about ambiguity
2023, NeuroImage
Cortical task control networks, including the cingulo-opercular (CO) network play a key role in decision-making across a variety of functional domains. In particular, the CO network functions in a performance reporting capacity that supports successful task performance, especially in response to errors and ambiguity. In two studies testing the contribution of the CO network to ambiguity processing, we presented a valence bias task in which masked clearly and ambiguously valenced emotional expressions were slowly revealed over several seconds. This slow reveal task design provides a window into the decision-making mechanisms as they unfold over the course of a trial. In the main study, the slow reveal task was administered to 32 young adults in the fMRI environment and BOLD time courses were extracted from regions of interest in three control networks. In a follow-up study, the task was administered to a larger, online sample (n = 81) using a more extended slow reveal design with additional unmasking frames. Positive judgments of surprised faces were uniquely accompanied by slower response times and strong, late activation in the CO network. These results support the initial negativity hypothesis, which posits that the default response to ambiguity is negative and positive judgments are associated with a more effortful controlled process, and additionally suggest that this controlled process is mediated by the CO network. Moreover, ambiguous trials were characterized by a second CO response at the end of the trial, firmly placing CO function late in the decision-making process.
Blink- and saccade-related suppression effects in early visual areas of the human brain: Intracranial EEG investigations during natural viewing conditions
2021, NeuroImage
Blinks and saccades, both ubiquitous in natural viewing conditions, cause rapid changes of visual inputs that are hardly consciously perceived. The neural dynamics in early visual areas of the human brain underlying this remarkable visual stability are still incompletely understood. We used electrocorticography (ECoG) from electrodes directly implanted on the human early visual areas V1, V2, V3d/v, V4d/v and the fusiform gyrus to investigate blink- and saccade-related neuronal suppression effects during non-experimental, free viewing conditions. We found a characteristic, biphasic, broadband gamma power decrease-increase pattern in all investigated visual areas. During saccades, a decrease in gamma power clearly preceded eye movement onset, at least in V1. This may indicate that cortical information processing is actively suppressed in human early visual areas before and during saccades, which then possibly mediates perceptual visual suppression. The following eye movement offset-related increase in gamma power may indicate the recovery of visual perception and the resumption of visual processing.
Human sensory cortex structure and top-down controlling brain network determine individual differences in perceptual alternations
2017, Neuroscience Letters
Bistable perception is a type of subjective perception that spontaneously alternates between two perceptual interpretations of an ambiguous sensory input. Past functional magnetic resonance imaging (fMRI) studies have examined the activation patterns underlying bistable perception, yet the variability between individuals in the alternations is not well understood. Therefore, voxel-based morphometry (VBM) was introduced in this study to correlate the GM of the sensory cortex with the alternations of Rubin face-vase illusion in a large group of young adults. We found that the GM volume and density (GMV/GMD) of the left fusiform face area (FFA) were significantly positively correlated with the alternations. Next, Granger causality analysis (GCA) was introduced to investigate the top-down modulation from high-level areas to the sensory cortex using resting-state fMRI data. Correlations between the perceptual alternations and Granger causalities showed that the top-down modulations from high-level brain regions, such as the superior parietal lobule (SPL) to the left FFA, were positive. Together, these findings indicated that the anatomical structure of the face-selective area may determine individual alternations of the Rubin face-vase illusion. This process may be controlled by a high-level cortex associated with attentional modulation, such as the SPL or Posterior Cingulate Cortex (PCC).
Identifying neural correlates of visual consciousness with ALE meta-analyses
2015, NeuroImage
Citation Excerpt :
Given that four studies are not sufficient to conduct a meaningful separate meta-analysis, we decided to focus on the 21 studies contrasting subliminal with conscious visual processing. Two of the 21 studies were excluded because they did not control for button press as sensorimotor confound (Freeman et al., 2012; Sterzer et al., 2002). The final pool thus consisted of 19 studies encompassing 211 foci and 225 subjects.
Neural correlates of consciousness (NCC) have been a topic of study for nearly two decades. In functional imaging studies, several regions have been proposed to constitute possible candidates for NCC, but as of yet, no quantitative summary of the literature on NCC has been done. The question whether single (striate or extrastriate) regions or a network consisting of extrastriate areas that project directly to fronto-parietal regions are necessary and sufficient neural correlates for visual consciousness is still highly debated [e.g., Rees et al., 2002, Nat Rev. Neurosci 3, 261–270; Tong, 2003, Nat Rev. Neurosci 4, 219–229]. The aim of this work was to elucidate this issue and give a synopsis of the present state of the art by conducting systematic and quantitative meta-analyses across functional magnetic resonance imaging (fMRI) studies using several standard paradigms for conscious visual perception. In these paradigms, consciousness is operationalized via perceptual changes, while the visual stimulus remains invariant. An activation likelihood estimation (ALE) meta-analysis was performed, representing the best approach for voxel-wise meta-analyses to date. In addition to computing a meta-analysis across all paradigms, separate meta-analyses on bistable perception and masking paradigms were conducted to assess whether these paradigms show common or different NCC. For the overall meta-analysis, we found significant clusters of activation in inferior and middle occipital gyrus; fusiform gyrus; inferior temporal gyrus; caudate nucleus; insula; inferior, middle, and superior frontal gyri; precuneus; as well as in inferior and superior parietal lobules. These results suggest a subcortical-extrastriate-fronto-parietal network rather than a single region that constitutes the necessary NCC. The results of our exploratory paradigm-specific meta-analyses suggest that this subcortical-extrastriate-fronto-parietal network might be differentially activated as a function of the paradigms used to probe for NCC.
Neural Correlates of Visual Consciousness
2015, The Neurology of Consciousness: Cognitive Neuroscience and Neuropathology
Vision is our primary sense, and seeing is accompanied by visual awareness or subjective experience of the visual world around us. Changes in the visual world often lead to changes in the content of visual awareness, and this is accompanied by changes in neural activity. However, not all neural activity associated with vision is correlated with changes in the contents of visual awareness. Indeed, much of the neural activity underpinning our ability to see remains unconscious and inaccessible to introspection. For example, the detailed computations underlying our ability to see three-dimensional depth are not apparent in awareness, but are just the end result of those computations. Thus, determining the neural correlates of the contents of visual awareness requires an empirical distinction to be made between neural activity that is correlated with the contents of visual awareness and that correlated only with unconscious processes. This chapter focuses on how recent studies of the visual system in humans have contributed to our emerging knowledge and understanding of the neural correlates of the contents of visual awareness.
Separable responses to error, ambiguity, and reaction time in cingulo-opercular task control regions
2014, NeuroImage
Citation Excerpt :
On the other hand, many studies have been interpreted to suggest that dACC/msFC activity is related to processes associated with decision uncertainty. In one line of work, the dACC/msFC appears to show responses to ambiguity in semantic (Thompson-Schill et al., 1997), visual motion (Sterzer et al., 2002), and face processing paradigms (Demos et al., 2004), as well as ambiguity in emotion (Neta et al., 2013). Similarly, the dACC/msFC has been widely thought to respond more in situations of conflict (Botvinick et al., 1999, 2001; Carter et al., 1998; MacLeod and MacDonald, 2000), particularly when the task requires a response relevant to that conflict (Milham et al., 2001).
The dorsal anterior cingulate (dACC), along with the closely affiliated anterior insula/frontal operculum, have been demonstrated to show three types of task control signals across a wide variety of tasks. One of these signals, a transient signal that is thought to represent performance feedback, shows greater activity to error than correct trials. Other work has found similar effects for uncertainty/ambiguity or conflict, though some argue that dACC activity is, instead, modulated primarily by other processes more reflected in reaction time. Here, we demonstrate that, rather than a single explanation, multiple information processing operations are crucial to characterizing the function of these brain regions, by comparing operations within a single paradigm. Participants performed two tasks in an fMRI experimental session: (1) deciding whether or not visually presented word pairs rhyme, and (2) rating auditorily presented single words as abstract or concrete. A pilot was used to identify ambiguous stimuli for both tasks (e.g., word pair: BASS/GRACE; single word: CHANGE). We found greater cingulo-opercular activity for errors and ambiguous trials than clear/correct trials, with a robust effect of reaction time. The effects of error and ambiguity remained when reaction time was regressed out, although the differences decreased. Further stepwise regression of response consensus (agreement across participants for each stimulus; a proxy for ambiguity) decreased differences between ambiguous and clear trials, but left error-related differences almost completely intact. These observations suggest that trial-wise responses in cingulo-opercular regions monitor multiple performance indices, including accuracy, ambiguity, and reaction time.

View all citing articles on Scopus

View full text

Regular ArticleNeural Correlates of Spontaneous Direction Reversals in Ambiguous Apparent Visual Motion

Abstract

Neuropsychologia

Trends Neurosci.

Neuropsychologia

Trends Cognit. Sci.

Neuropsychologia

Curr. Opin. Neurobiol.

Neuron.

Spatiotemporal activity of a cortical network for processing visual motion revealed by MEG and fMRI

J. Neurophysiol.

Effects of visual angle on perspective reversal for ambiguous patterns

Perception

Reversal time distribution in the perception of visual ambiguous stimuli

Kybernetik

The functional anatomy of attention to visual motion. A functional MRI study

Brain

Randomized event-related experimental designs allow for extremely rapid presentation rates using functional MRI

NeuroReport

The physiological basis of attentional modulation in extrastriate visual areas

Nat. Neurosci.

Frontoparietal cortical networks for directing attention and the eye to visual locations: Identical, independent, or overlapping neural systems?

Proc. Natl. Acad. Sci. USA

A PET study of visuospatial attention

J. Neurosci.

Human brain regions involved in direction discrimination

J. Neurophysiol.

Both sides of human cerebellum involved in preparation and execution of sequential movements

NeuroReport

A multimodal cortical network for the detection of changes in the sensory environment

Nat. Neurosci.

Multiple temporal components of optic flow responses in MST neurons

Exp. Brain Res.

Eye movement-related inhibition of primate visual neurons

Brain Res.

The kinetic occipital region in human visual cortex

Cereb. Cortex

The waggon-wheel effect

Perception

Speed of apparent motion and the wagon-wheel effect

Percept. Psychophys.

Statistical parametric maps in functional imaging: A general linear approach

Hum. Brain Mapp.

The constructive nature of vision: Direct evidence from functional magnetic resonance imaging studies of apparent motion and motion imagery

Eur. J. Neurosci.

Effect of task difficulty on cerebral blood flow during perceptual matching of faces

Hum. Brain Mapp.

Motion opponency in visual cortex

J. Neurosci.

Event-related functional magnetic resonance imaging: Modelling, inference and optimization

Philos. Trans. R. Soc. London B Biol. Sci.

Event-related fMRI

Hum. Brain Mapp.

Multistability and metastability in perceptual and brain dynamics

Regular Article
Neural Correlates of Spontaneous Direction Reversals in Ambiguous Apparent Visual Motion