Distinct neural mechanisms of spatial attention and expectation guide perceptual inference in a multisensory world

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Distinct neural mechanisms of spatial attention and expectation guide perceptual inference in a multisensory world. / Zuanazzi, Arianna; Noppeney, Uta.

In: The Journal of Neuroscience, Vol. 39, No. 12, 20.03.2019, p. 2301-2312.

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@article{f16b93e6261347bbb6d5fdbce6359d20,
title = "Distinct neural mechanisms of spatial attention and expectation guide perceptual inference in a multisensory world",
abstract = "Spatial attention (i.e., task-relevance) and expectation (i.e., signal probability) are two critical top-down mechanisms guiding perceptual inference. Spatial attention prioritizes processing of information at task-relevant locations. Spatial expectations encode the statistical structure of the environment. An unresolved question is how the brain allocates attention and forms expectations in a multisensory environment, where task-relevance and signal probability over space can differ across sensory modalities. We used functional magnetic resonance imaging in human participants (female and male) to investigate whether the brain encodes task-relevance and signal probability over space separately or interactively across sensory modalities. In a novel multisensory paradigm, we manipulated spatial attention and expectation selectively in audition and assessed their effects on behavioral and neural responses to auditory and visual stimuli. Our results show that both auditory and visual stimuli increased activations in a right-lateralized frontoparietal system, when they were presented at locations that were task-irrelevant in audition. Yet, only auditory stimuli increased activations in the medial prefrontal cortex when presented at expected locations and in audiovisual and frontoparietal cortices signaling a prediction error when presented at unexpected locations. This dissociation in multisensory generalization for attention and expectation effects shows that the brain controls attentional resources interactively across the senses but encodes the statistical structure of the environment as spatial expectations independently for each sensory system. Our results demonstrate that spatial attention and expectation engage partly overlapping neural systems via distinct mechanisms to guide perceptual inference in a multisensory world. SIGNIFICANCE STATEMENT In our natural environment the brain is exposed to a constant influx of signals through all our senses. How does the brain allocate attention and form spatial expectations in this multisensory environment? Because observers need to respond to stimuli regardless of their sensory modality, they may allocate attentional resources and encode the probability of events jointly across the senses. This psychophysics and neuroimaging study shows that the brain controls attentional resources interactively across the senses via a frontoparietal system but encodes the statistical structure of the environment independently for each sense in sensory and frontoparietal areas. Thus, spatial attention and expectation engage partly overlapping neural systems via distinct mechanisms to guide perceptual inference in a multisensory world. ",
keywords = "Attention, Expectation, FMRI, Multisensory, Perceptual decisions, Space",
author = "Arianna Zuanazzi and Uta Noppeney",
note = "Copyright {\textcopyright} 2019 the authors",
year = "2019",
month = mar,
day = "20",
doi = "10.1523/JNEUROSCI.2873-18.2019",
language = "English",
volume = "39",
pages = "2301--2312",
journal = "The Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "12",

}

RIS

TY - JOUR

T1 - Distinct neural mechanisms of spatial attention and expectation guide perceptual inference in a multisensory world

AU - Zuanazzi, Arianna

AU - Noppeney, Uta

N1 - Copyright © 2019 the authors

PY - 2019/3/20

Y1 - 2019/3/20

N2 - Spatial attention (i.e., task-relevance) and expectation (i.e., signal probability) are two critical top-down mechanisms guiding perceptual inference. Spatial attention prioritizes processing of information at task-relevant locations. Spatial expectations encode the statistical structure of the environment. An unresolved question is how the brain allocates attention and forms expectations in a multisensory environment, where task-relevance and signal probability over space can differ across sensory modalities. We used functional magnetic resonance imaging in human participants (female and male) to investigate whether the brain encodes task-relevance and signal probability over space separately or interactively across sensory modalities. In a novel multisensory paradigm, we manipulated spatial attention and expectation selectively in audition and assessed their effects on behavioral and neural responses to auditory and visual stimuli. Our results show that both auditory and visual stimuli increased activations in a right-lateralized frontoparietal system, when they were presented at locations that were task-irrelevant in audition. Yet, only auditory stimuli increased activations in the medial prefrontal cortex when presented at expected locations and in audiovisual and frontoparietal cortices signaling a prediction error when presented at unexpected locations. This dissociation in multisensory generalization for attention and expectation effects shows that the brain controls attentional resources interactively across the senses but encodes the statistical structure of the environment as spatial expectations independently for each sensory system. Our results demonstrate that spatial attention and expectation engage partly overlapping neural systems via distinct mechanisms to guide perceptual inference in a multisensory world. SIGNIFICANCE STATEMENT In our natural environment the brain is exposed to a constant influx of signals through all our senses. How does the brain allocate attention and form spatial expectations in this multisensory environment? Because observers need to respond to stimuli regardless of their sensory modality, they may allocate attentional resources and encode the probability of events jointly across the senses. This psychophysics and neuroimaging study shows that the brain controls attentional resources interactively across the senses via a frontoparietal system but encodes the statistical structure of the environment independently for each sense in sensory and frontoparietal areas. Thus, spatial attention and expectation engage partly overlapping neural systems via distinct mechanisms to guide perceptual inference in a multisensory world.

AB - Spatial attention (i.e., task-relevance) and expectation (i.e., signal probability) are two critical top-down mechanisms guiding perceptual inference. Spatial attention prioritizes processing of information at task-relevant locations. Spatial expectations encode the statistical structure of the environment. An unresolved question is how the brain allocates attention and forms expectations in a multisensory environment, where task-relevance and signal probability over space can differ across sensory modalities. We used functional magnetic resonance imaging in human participants (female and male) to investigate whether the brain encodes task-relevance and signal probability over space separately or interactively across sensory modalities. In a novel multisensory paradigm, we manipulated spatial attention and expectation selectively in audition and assessed their effects on behavioral and neural responses to auditory and visual stimuli. Our results show that both auditory and visual stimuli increased activations in a right-lateralized frontoparietal system, when they were presented at locations that were task-irrelevant in audition. Yet, only auditory stimuli increased activations in the medial prefrontal cortex when presented at expected locations and in audiovisual and frontoparietal cortices signaling a prediction error when presented at unexpected locations. This dissociation in multisensory generalization for attention and expectation effects shows that the brain controls attentional resources interactively across the senses but encodes the statistical structure of the environment as spatial expectations independently for each sensory system. Our results demonstrate that spatial attention and expectation engage partly overlapping neural systems via distinct mechanisms to guide perceptual inference in a multisensory world. SIGNIFICANCE STATEMENT In our natural environment the brain is exposed to a constant influx of signals through all our senses. How does the brain allocate attention and form spatial expectations in this multisensory environment? Because observers need to respond to stimuli regardless of their sensory modality, they may allocate attentional resources and encode the probability of events jointly across the senses. This psychophysics and neuroimaging study shows that the brain controls attentional resources interactively across the senses via a frontoparietal system but encodes the statistical structure of the environment independently for each sense in sensory and frontoparietal areas. Thus, spatial attention and expectation engage partly overlapping neural systems via distinct mechanisms to guide perceptual inference in a multisensory world.

KW - Attention

KW - Expectation

KW - FMRI

KW - Multisensory

KW - Perceptual decisions

KW - Space

UR - http://www.scopus.com/inward/record.url?scp=85063617677&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.2873-18.2019

DO - 10.1523/JNEUROSCI.2873-18.2019

M3 - Article

C2 - 30659086

VL - 39

SP - 2301

EP - 2312

JO - The Journal of Neuroscience

JF - The Journal of Neuroscience

SN - 0270-6474

IS - 12

ER -