Pivotal role of hMT+ in long‐range disambiguation of interhemispheric bistable surface motion

Duarte, João Valente; Costa, Gabriel Nascimento; Martins, Ricardo; Castelo‐Branco, Miguel

doi:10.1002/hbm.23701

Title: Pivotal role of hMT+ in long‐range disambiguation of interhemispheric bistable surface motion

Abstract

Abstract It remains an open question whether long‐range disambiguation of ambiguous surface motion can be achieved in early visual cortex or instead in higher level regions, which concerns object/surface segmentation/integration mechanisms. We used a bistable moving stimulus that can be perceived as a pattern comprehending both visual hemi‐fields moving coherently downward or as two widely segregated nonoverlapping component objects (in each visual hemi‐field) moving separately inward. This paradigm requires long‐range integration across the vertical meridian leading to interhemispheric binding. Our fMRI study ( n = 30) revealed a close relation between activity in hMT+ and perceptual switches involving interhemispheric segregation/integration of motion signals, crucially under nonlocal conditions where components do not overlap and belong to distinct hemispheres. Higher signal changes were found in hMT+ in response to spatially segregated component (incoherent) percepts than to pattern (coherent) percepts. This did not occur in early visual cortex, unlike apparent motion, which does not entail surface segmentation. We also identified a role for top–down mechanisms in state transitions. Deconvolution analysis of switch‐related changes revealed prefrontal, insula, and cingulate areas, with the right superior parietal lobule (SPL) being particularly involved. We observed that directed influences could emerge either from left or right hMT+ during bistablemore »« less

Authors:

^[1];

^[1]

CiBIT, ICNAS, Institute for Biomedical Imaging in Life Sciences (IBILI) ‐ Faculty of Medicine, University of Coimbra Portugal

Publication Date:: Wed Jun 28 00:00:00 EDT 2017

Sponsoring Org.:: USDOE

OSTI Identifier:: 1389142

Resource Type:: Publisher's Accepted Manuscript

Journal Name:: Human Brain Mapping

Additional Journal Information:: Journal Name: Human Brain Mapping Journal Volume: 38 Journal Issue: 10; Journal ID: ISSN 1065-9471

Publisher:: Wiley Blackwell (John Wiley & Sons)

Country of Publication:: United States

Language:: English

Citation Formats


                    Duarte, João Valente, Costa, Gabriel Nascimento, Martins, Ricardo, and Castelo‐Branco, Miguel. Pivotal role of hMT+ in long‐range disambiguation of interhemispheric bistable surface motion.  United States: N. p., 2017. 
Web.  doi:10.1002/hbm.23701.

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                    Duarte, João Valente, Costa, Gabriel Nascimento, Martins, Ricardo, & Castelo‐Branco, Miguel. Pivotal role of hMT+ in long‐range disambiguation of interhemispheric bistable surface motion.  United States.  https://doi.org/10.1002/hbm.23701

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                    Duarte, João Valente, Costa, Gabriel Nascimento, Martins, Ricardo, and Castelo‐Branco, Miguel. Wed .  
"Pivotal role of hMT+ in long‐range disambiguation of interhemispheric bistable surface motion".  United States.  https://doi.org/10.1002/hbm.23701.

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@article{osti_1389142,

  title        = {Pivotal role of hMT+ in long‐range disambiguation of interhemispheric bistable surface motion},

  author       = {Duarte, João Valente and Costa, Gabriel Nascimento and Martins, Ricardo and Castelo‐Branco, Miguel},

  abstractNote = {Abstract It remains an open question whether long‐range disambiguation of ambiguous surface motion can be achieved in early visual cortex or instead in higher level regions, which concerns object/surface segmentation/integration mechanisms. We used a bistable moving stimulus that can be perceived as a pattern comprehending both visual hemi‐fields moving coherently downward or as two widely segregated nonoverlapping component objects (in each visual hemi‐field) moving separately inward. This paradigm requires long‐range integration across the vertical meridian leading to interhemispheric binding. Our fMRI study ( n  = 30) revealed a close relation between activity in hMT+ and perceptual switches involving interhemispheric segregation/integration of motion signals, crucially under nonlocal conditions where components do not overlap and belong to distinct hemispheres. Higher signal changes were found in hMT+ in response to spatially segregated component (incoherent) percepts than to pattern (coherent) percepts. This did not occur in early visual cortex, unlike apparent motion, which does not entail surface segmentation. We also identified a role for top–down mechanisms in state transitions. Deconvolution analysis of switch‐related changes revealed prefrontal, insula, and cingulate areas, with the right superior parietal lobule (SPL) being particularly involved. We observed that directed influences could emerge either from left or right hMT+ during bistable motion integration/segregation. SPL also exhibited significant directed functional connectivity with hMT+, during perceptual state maintenance (Granger causality analysis). Our results suggest that long‐range interhemispheric binding of ambiguous motion representations mainly reflect bottom–up processes from hMT+ during perceptual state maintenance. In contrast, state transitions maybe influenced by high‐level regions such as the SPL. Hum Brain Mapp 38:4882–4897, 2017 . © 2017 Wiley Periodicals, Inc.},

  doi          = {10.1002/hbm.23701},

  journal      = {Human Brain Mapping},

  number       = 10,

  volume       = 38,

  place        = {United States},

  year         = {Wed Jun 28 00:00:00 EDT 2017},

  month        = {Wed Jun 28 00:00:00 EDT 2017}

}

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Leopold, David A.; Logothetis, Nikos K.
Trends in Cognitive Sciences, Vol. 3, Issue 7
DOI: 10.1016/S1364-6613(99)01332-7

Common fronto-parietal activity in attention, memory, and consciousness: Shared demands on integration?
journal, June 2005

Naghavi, Hamid Reza; Nyberg, Lars
Consciousness and Cognition, Vol. 14, Issue 2
DOI: 10.1016/j.concog.2004.10.003

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Title: Pivotal role of hMT+ in long‐range disambiguation of interhemispheric bistable surface motion

Abstract

Citation Formats

The Role of Frontal and Parietal Brain Areas in Bistable Perception journal, July 2011

End-Stopping and the Aperture Problem journal, August 2003

Reversal time distribution in the perception of visual ambiguous stimuli journal, March 1972

Perceptual decision-making difficulty modulates feedforward effective connectivity to the dorsolateral prefrontal cortex journal, September 2015

Functional parcellation of the operculo-insular cortex in perceptual decision making: An fMRI study journal, December 2012

The VideoToolbox software for visual psychophysics: transforming numbers into movies journal, January 1997

The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution journal, September 2011

Working memory load influences perceptual ambiguity by competing for fronto-parietal attentional resources journal, November 2016

Phenomenal coherence of moving visual patterns journal, December 1982

Analysis of functional MRI time-series journal, January 1994

Disrupting Parietal Function Prolongs Dominance Durations in Binocular Rivalry journal, December 2010

Right parietal TMS shortens dominance durations in binocular rivalry journal, September 2010

Activity patterns in human motion-sensitive areas depend on the interpretation of global motion journal, October 2002

A model of neuronal responses in visual area MT journal, March 1998

Apparent Motion: Event-Related Functional Magnetic Resonance Imaging of Perceptual Switches and States journal, May 2002

Neural Correlates of Spontaneous Direction Reversals in Ambiguous Apparent Visual Motion journal, April 2002

Analyzing effective connectivity with functional magnetic resonance imaging journal, May 2010

The kinetic occipital region in human visual cortex journal, April 1997

Primary visual cortex activation on the path of apparent motion is mediated by feedback from hMT+/V5 journal, September 2006

Type of Featural Attention Differentially Modulates hMT + Responses to Illusory Motion Aftereffects journal, November 2009

The Retinotopic Organization of the Human Middle Temporal Area MT/V5 and Its Cortical Neighbors journal, July 2010

Neural basis of stable perception of an ambiguous apparent motion stimulus journal, March 2009

Illusory motion reversal is caused by rivalry, not by perceptual snapshots of the visual field journal, October 2004

Granger causality analysis of fMRI BOLD signals is invariant to hemodynamic convolution but not downsampling journal, January 2013

Decoding pattern motion information in V1 journal, August 2014

The Representation of Behavioral Choice for Motion in Human Visual Cortex journal, November 2007

The Timing of Feedback to Early Visual Cortex in the Perception of Long-Range Apparent Motion journal, November 2008

Stable perception of visually ambiguous patterns journal, May 2002

Visual motion perception. journal, March 1995

Covariation of activity in visual and prefrontal cortex associated with subjective visual perception journal, February 1999

Local and Global Representations of Velocity: Transparency, Opponency, and Global Direction Perception journal, August 1997

Structural and functional fractionation of right superior parietal cortex in bistable perception journal, February 2011

Spatiotemporal energy models for the perception of motion journal, January 1985

Analysing connectivity with Granger causality and dynamic causal modelling journal, April 2013

Pattern motion selectivity in population responses of area 18 journal, October 2006

Enduring Interest in Perceptual Ambiguity: Alternating Views of Reversible Figures. journal, January 2004

The contribution of one-dimensional motion mechanisms to the perceived direction of drifting plaids and their aftereffects journal, July 1994

The activity in the anterior insulae is modulated by perceptual decision-making difficulty journal, July 2016

Über visuell wahrgenommene Bewegungsrichtung journal, December 1935

Neuromagnetic correlates of visual motion coherence journal, December 2005

Spatio-temporal prediction and inference by V1 neurons: Spatio-temporal integration in V1 journal, August 2007

The kinetic occipital (KO) region in man: an fMRI study journal, October 1997

Distributions of alternation rates in various forms of bistable perception journal, April 2005

Visual Response Properties of Striate Cortical Neurons Projecting to Area MT in Macaque Monkeys journal, December 1996

The Nature of V1 Neural Responses to 2D Moving Patterns Depends on Receptive-Field Structure in the Marmoset Monkey journal, August 2003

Mapping the bilateral visual integration by EEG and fMRI journal, July 2009

A neural basis for inference in perceptual ambiguity journal, December 2006

The Functional Neuroanatomy of Target Detection: An fMRI Study of Visual and Auditory Oddball Tasks journal, December 1999

The linear impact of concurrent working memory load on dynamics of Necker cube perceptual reversals journal, January 2014

Beyond Junctions: Nonlocal form Constraints on Motion Interpretation journal, August 2001

Investigating directed cortical interactions in time-resolved fMRI data using vector autoregressive modeling and Granger causality mapping journal, December 2003

Primary Visual Cortex Activity along the Apparent-Motion Trace Reflects Illusory Perception journal, July 2005

Voluntary Attention Modulates fMRI Activity in Human MT–MST journal, April 1997

Functional and Effective Connectivity: A Review journal, January 2011

Decoding of coherent but not incoherent motion signals in early dorsal visual cortex journal, May 2011

Perceptual dominance time distributions in multistable visual perception journal, April 2004

Long-range interactions in the spatial integration of motion signals journal, January 1999

Brain activity dynamics in human parietal regions during spontaneous switches in bistable perception journal, February 2015

Imagery of a moving object: The role of occipital cortex and human MT/V5+ journal, January 2010

Human brain activity during spontaneously reversing perception of ambiguous figures journal, December 1998

Neural synchrony correlates with surface segregation rules journal, June 2000

The Brain Structural Hub of Interhemispheric Information Integration for Visual Motion Perception journal, June 2011

Functional Analysis of V3A and Related Areas in Human Visual Cortex journal, September 1997

The assessment and analysis of handedness: The Edinburgh inventory journal, March 1971

Voluntary control of long-range motion integration via selective attention to context journal, August 2008

Deconvolution of Impulse Response in Event-Related BOLD fMRI1 journal, April 1999

Pattern-motion responses in human visual cortex journal, December 2001

The Psychophysics Toolbox journal, January 1997

Interhemispheric Connections Shape Subjective Experience of Bistable Motion journal, September 2011

On the Functional Relevance of Frontal Cortex for Passive and Voluntarily Controlled Bistable Vision journal, March 2011

Mapping directed influence over the brain using Granger causality and fMRI journal, March 2005

No-Report Paradigms: Extracting the True Neural Correlates of Consciousness journal, December 2015

Neural Correlates of Perceptual Rivalry in the Human Brain journal, June 1998

Peripheral Influences on Motion Integration in Foveal Vision Are Modulated by Central Local Ambiguity and Center-Surround Congruence journal, February 2009

Frontoparietal Cortex Mediates Perceptual Transitions in Bistable Perception journal, October 2013

A cortical network that marks the moment when conscious representations are updated journal, December 2015

Negligible fronto-parietal BOLD activity accompanying unreportable switches in bistable perception journal, October 2015

The Role of Frontal and Parietal Brain Areas in Bistable Perception
journal, July 2011

End-Stopping and the Aperture Problem
journal, August 2003

Reversal time distribution in the perception of visual ambiguous stimuli
journal, March 1972

Perceptual decision-making difficulty modulates feedforward effective connectivity to the dorsolateral prefrontal cortex
journal, September 2015

Functional parcellation of the operculo-insular cortex in perceptual decision making: An fMRI study
journal, December 2012

The VideoToolbox software for visual psychophysics: transforming numbers into movies
journal, January 1997

The identification of interacting networks in the brain using fMRI: Model selection, causality and deconvolution
journal, September 2011

Working memory load influences perceptual ambiguity by competing for fronto-parietal attentional resources
journal, November 2016

Phenomenal coherence of moving visual patterns
journal, December 1982

Analysis of functional MRI time-series
journal, January 1994

Disrupting Parietal Function Prolongs Dominance Durations in Binocular Rivalry
journal, December 2010

Right parietal TMS shortens dominance durations in binocular rivalry
journal, September 2010

Activity patterns in human motion-sensitive areas depend on the interpretation of global motion
journal, October 2002

A model of neuronal responses in visual area MT
journal, March 1998

Apparent Motion: Event-Related Functional Magnetic Resonance Imaging of Perceptual Switches and States
journal, May 2002

Neural Correlates of Spontaneous Direction Reversals in Ambiguous Apparent Visual Motion
journal, April 2002

Analyzing effective connectivity with functional magnetic resonance imaging
journal, May 2010

The kinetic occipital region in human visual cortex
journal, April 1997

Primary visual cortex activation on the path of apparent motion is mediated by feedback from hMT+/V5
journal, September 2006

Type of Featural Attention Differentially Modulates hMT ⁺ Responses to Illusory Motion Aftereffects
journal, November 2009

The Retinotopic Organization of the Human Middle Temporal Area MT/V5 and Its Cortical Neighbors
journal, July 2010

Neural basis of stable perception of an ambiguous apparent motion stimulus
journal, March 2009

Illusory motion reversal is caused by rivalry, not by perceptual snapshots of the visual field
journal, October 2004

Granger causality analysis of fMRI BOLD signals is invariant to hemodynamic convolution but not downsampling
journal, January 2013

Decoding pattern motion information in V1
journal, August 2014

The Representation of Behavioral Choice for Motion in Human Visual Cortex
journal, November 2007

The Timing of Feedback to Early Visual Cortex in the Perception of Long-Range Apparent Motion
journal, November 2008

Stable perception of visually ambiguous patterns
journal, May 2002

Visual motion perception.
journal, March 1995

Covariation of activity in visual and prefrontal cortex associated with subjective visual perception
journal, February 1999

Local and Global Representations of Velocity: Transparency, Opponency, and Global Direction Perception
journal, August 1997

Structural and functional fractionation of right superior parietal cortex in bistable perception
journal, February 2011

Spatiotemporal energy models for the perception of motion
journal, January 1985

Analysing connectivity with Granger causality and dynamic causal modelling
journal, April 2013

Pattern motion selectivity in population responses of area 18
journal, October 2006

Enduring Interest in Perceptual Ambiguity: Alternating Views of Reversible Figures.
journal, January 2004

The contribution of one-dimensional motion mechanisms to the perceived direction of drifting plaids and their aftereffects
journal, July 1994

The activity in the anterior insulae is modulated by perceptual decision-making difficulty
journal, July 2016

Über visuell wahrgenommene Bewegungsrichtung
journal, December 1935

Neuromagnetic correlates of visual motion coherence
journal, December 2005

Spatio-temporal prediction and inference by V1 neurons: Spatio-temporal integration in V1
journal, August 2007

The kinetic occipital (KO) region in man: an fMRI study
journal, October 1997

Distributions of alternation rates in various forms of bistable perception
journal, April 2005

Visual Response Properties of Striate Cortical Neurons Projecting to Area MT in Macaque Monkeys
journal, December 1996

The Nature of V1 Neural Responses to 2D Moving Patterns Depends on Receptive-Field Structure in the Marmoset Monkey
journal, August 2003

Mapping the bilateral visual integration by EEG and fMRI
journal, July 2009

A neural basis for inference in perceptual ambiguity
journal, December 2006

The Functional Neuroanatomy of Target Detection: An fMRI Study of Visual and Auditory Oddball Tasks
journal, December 1999

The linear impact of concurrent working memory load on dynamics of Necker cube perceptual reversals
journal, January 2014

Beyond Junctions: Nonlocal form Constraints on Motion Interpretation
journal, August 2001

Investigating directed cortical interactions in time-resolved fMRI data using vector autoregressive modeling and Granger causality mapping
journal, December 2003

Primary Visual Cortex Activity along the Apparent-Motion Trace Reflects Illusory Perception
journal, July 2005

Voluntary Attention Modulates fMRI Activity in Human MT–MST
journal, April 1997

Functional and Effective Connectivity: A Review
journal, January 2011

Decoding of coherent but not incoherent motion signals in early dorsal visual cortex
journal, May 2011

Perceptual dominance time distributions in multistable visual perception
journal, April 2004

Long-range interactions in the spatial integration of motion signals
journal, January 1999

Brain activity dynamics in human parietal regions during spontaneous switches in bistable perception
journal, February 2015

Imagery of a moving object: The role of occipital cortex and human MT/V5+
journal, January 2010

Human brain activity during spontaneously reversing perception of ambiguous figures
journal, December 1998

Neural synchrony correlates with surface segregation rules
journal, June 2000

The Brain Structural Hub of Interhemispheric Information Integration for Visual Motion Perception
journal, June 2011

Functional Analysis of V3A and Related Areas in Human Visual Cortex
journal, September 1997

The assessment and analysis of handedness: The Edinburgh inventory
journal, March 1971

Voluntary control of long-range motion integration via selective attention to context
journal, August 2008

Deconvolution of Impulse Response in Event-Related BOLD fMRI1
journal, April 1999

Pattern-motion responses in human visual cortex
journal, December 2001

The Psychophysics Toolbox
journal, January 1997

Interhemispheric Connections Shape Subjective Experience of Bistable Motion
journal, September 2011

On the Functional Relevance of Frontal Cortex for Passive and Voluntarily Controlled Bistable Vision
journal, March 2011

Mapping directed influence over the brain using Granger causality and fMRI
journal, March 2005

No-Report Paradigms: Extracting the True Neural Correlates of Consciousness
journal, December 2015

Neural Correlates of Perceptual Rivalry in the Human Brain
journal, June 1998

Peripheral Influences on Motion Integration in Foveal Vision Are Modulated by Central Local Ambiguity and Center-Surround Congruence
journal, February 2009

Frontoparietal Cortex Mediates Perceptual Transitions in Bistable Perception
journal, October 2013

A cortical network that marks the moment when conscious representations are updated
journal, December 2015

Negligible fronto-parietal BOLD activity accompanying unreportable switches in bistable perception
journal, October 2015

The Size and Number of Plaid Blobs Mediate the Misperception of Type-II Plaid Direction
journal, January 1997

Functional Connectivity Patterns of Visual Cortex Reflect its Anatomical Organization
journal, August 2015

Human MT+ mediates perceptual filling-in during apparent motion
journal, April 2004