Dissecting neural circuits for multisensory integration and crossmodal processing

Yau, Jeffrey M.; DeAngelis, Gregory C.; Angelaki, Dora E.

doi:10.1098/rstb.2014.0203

Cited by 57 publications

(51 citation statements)

References 143 publications

(193 reference statements)

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“…These co-activations are thought to reflect the binding of information-linked neural representations via the crossmodal spread of spatial attention [38,39] or feature-based attention [40–42]. The causal manipulation of activity in one sensory system using non-invasive brain stimulation can modulate processing in a different sensory modality [43], implying an interactive connectivity between sensory cortical systems. Our results demonstrate that the interactive coupling between cortical systems which support different sensory modalities is modulated by selective attention.…”

Section: Discussionmentioning

confidence: 99%

Selective Attention Gates the Interactive Crossmodal Coupling between Perceptual Systems

2018

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Sensory cortical systems often activate in parallel, even when stimulation is experienced through a single sensory modality [1-3]. Co-activations may reflect the interactive coupling between information-linked cortical systems or merely parallel but independent sensory processing. We report causal evidence consistent with the hypothesis that human somatosensory cortex (S1), which co-activates with auditory cortex during the processing of vibrations and textures [4-9], interactively couples to cortical systems that support auditory perception. In a series of behavioral experiments, we used transcranial magnetic stimulation (TMS) to probe interactions between the somatosensory and auditory perceptual systems as we manipulated attention state. Acute TMS over S1 impairs auditory frequency perception when subjects simultaneously attend to auditory and tactile frequency, but not when attention is directed to audition alone. Auditory frequency perception is unaffected by TMS over visual cortex, thus confirming the privileged interactions between the somatosensory and auditory systems in temporal frequency processing [10-13]. Our results provide a key demonstration that selective attention can modulate the functional properties of cortical systems thought to support specific sensory modalities. The gating of crossmodal coupling by selective attention may critically support multisensory interactions and feature-specific perception.

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Section: Discussionmentioning

confidence: 99%

Selective Attention Gates the Interactive Crossmodal Coupling between Perceptual Systems

2018

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“…The afterresponse suggests two adaptation processes with time constants of 15 s and 300 s, and even longer periods of stimulation suggest a third on the order of hour(s) [44]. Since our VOR adaptation timescales are close to those for podokinetic adaptation [45], one can speculate the vestibular and podokinetic systems share similar central adaptation operators within a central balance network that incorporates multiple sensory signals [4, 46, 47]. …”

Section: Discussionmentioning

confidence: 99%

Multiple Time Courses of Vestibular Set-Point Adaptation Revealed by Sustained Magnetic Field Stimulation of the Labyrinth

et al. 2016

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SUMMARY A major focus in neurobiology is how the brain adapts its motor behavior to changes in its internal and external environments [1, 2]. Much is known about adaptively optimizing the amplitude and direction of eye and limb movements, for example, but little is known about another essential form of learning, “set-point” adaptation. Set-point adaptation balances tonic activity so that reciprocally acting, agonist and antagonist muscles have a stable platform from which to launch accurate movements. Here, we use the vestibulo-ocular reflex—a simple behavior that stabilizes the position of the eye while the head is moving—to investigate how tonic activity is adapted toward a new set point to prevent eye drift when the head is still [3, 4]. Set-point adaptation was elicited with magneto-hydrodynamic vestibular stimulation (MVS) by placing normal humans in a 7T MRI for 90 min. MVS is ideal for prolonged labyrinthine activation because it mimics constant head acceleration and induces a sustained nystagmus similar to natural vestibular lesions [5, 6]. The MVS-induced nystagmus diminished slowly but incompletely over multiple timescales. We propose a new adaptation hypothesis, using a cascade of imperfect mathematical integrators, that reproduces the response to MVS (and more natural chair rotations), including the gradual decrease in nystagmus as the set point changes over progressively longer time courses. MVS set-point adaptation is a biological model with applications to basic neurophysiological research into all types of movements [7], functional brain imaging [8], and treatment of vestibular and higher-level attentional disorders by introducing new biases to counteract pathological ones [9].

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“…Integrating signals across sensory modalities can therefore reduce the inherent uncertainty within any sensory estimate and so improve performance in perceptual decisionmaking tasks. In the mammalian brain, the neural processes underlying decision-making [3,4] and multisensory integration [5][6][7] have become increasingly well understood but remain largely independent lines of investigation. In particular, it remains an open question at what point(s) in the decision-making process information is combined across modalities.…”

Section: Introductionmentioning

confidence: 99%

“…For example, it is possible that neurons in sensory areas integrating cross-modal stimuli make no contribution to decision-making. This issue cannot be addressed with behavioural neurophysiology or neuroimaging alone and requires neural manipulation to establish the causal effects of perturbing multisensory integration [7]. So far, causal contributions of both sensory and higher order areas to multisensory integration have been shown in humans [39][40][41] and other animals [26,[42][43][44].…”

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confidence: 98%

Where are multisensory signals combined for perceptual decision-making?

Bizley¹,

Jones²,

Town³

2016

Current Opinion in Neurobiology

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Multisensory integration is observed in many subcortical and cortical locations including primary and non-primary sensory cortex, and higher cortical areas including frontal and parietal cortex. During unisensory perceptual tasks many of these same brain areas show neural signatures associated with decision-making. It is unclear whether multisensory representations in sensory cortex directly inform decision-making in a multisensory task, or if cross-modal signals are only combined after the accumulation of unisensory evidence at a final decision-making stage in higher cortical areas. Manipulations of neuronal activity are required to establish causal roles for given brain regions in multisensory perceptual decision-making, and so far indicate that distributed networks underlie multisensory decision-making. Understanding multisensory integration requires synthesis of small-scale pathway specific and large-scale network level manipulations.

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Dissecting neural circuits for multisensory integration and crossmodal processing

Cited by 57 publications

References 143 publications

Selective Attention Gates the Interactive Crossmodal Coupling between Perceptual Systems

Selective Attention Gates the Interactive Crossmodal Coupling between Perceptual Systems

Multiple Time Courses of Vestibular Set-Point Adaptation Revealed by Sustained Magnetic Field Stimulation of the Labyrinth

Where are multisensory signals combined for perceptual decision-making?

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