Development of multisensory integration from the perspective of the individual neuron

Stein, Barry E.; Stanford, Terrence R.; Rowland, Benjamin A.

doi:10.1038/nrn3742

Cited by 329 publications

(296 citation statements)

References 167 publications

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“…Studies of visual (55) and somatosensory (30,53) pathways demonstrate the presence of thalamic bursting in awake and attentive states, implying that bursting activity modulates sensory perception. Intermittent activation of multiple long-range circuits to integrate major sensory cortices suggests that multisensory integration is essential to shape sensory perceptions that could not otherwise be achieved with only one sense (56,57). This premise raises an intriguing proposition that excitatory long-range projections and their dynamic interactions are recruited during low-frequency thalamic stimulation through burst activity propagation from VPM to S1 and, possibly, to other sensory cortices.…”

Section: Discussionmentioning

confidence: 99%

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Leong

Chan

Gao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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One challenge in contemporary neuroscience is to achieve an integrated understanding of the large-scale brain-wide interactions, particularly the spatiotemporal patterns of neural activity that give rise to functions and behavior. At present, little is known about the spatiotemporal properties of long-range neuronal networks. We examined brain-wide neural activity patterns elicited by stimulating ventral posteromedial (VPM) thalamo-cortical excitatory neurons through combined optogenetic stimulation and functional MRI (fMRI). We detected robust optogenetically evoked fMRI activation bilaterally in primary visual, somatosensory, and auditory cortices at low (1 Hz) but not high frequencies (5-40 Hz). Subsequent electrophysiological recordings indicated interactions over long temporal windows across thalamo-cortical, cortico-cortical, and interhemispheric callosal projections at low frequencies. We further observed enhanced visually evoked fMRI activation during and after VPM stimulation in the superior colliculus, indicating that visual processing was subcortically modulated by low-frequency activity originating from VPM. Stimulating posteromedial complex thalamo-cortical excitatory neurons also evoked brain-wide bloodoxygenation-level-dependent activation, although with a distinct spatiotemporal profile. Our results directly demonstrate that lowfrequency activity governs large-scale, brain-wide connectivity and interactions through long-range excitatory projections to coordinate the functional integration of remote brain regions. This low-frequency phenomenon contributes to the neural basis of long-range functional connectivity as measured by resting-state fMRI.fMRI | optogenetic | brain connectivity | low frequency | thalamus T he brain is a highly complex, interconnected structure with parallel and hierarchical networks distributed within and between neural systems (1, 2). This integrative architecture dictates the underlying principles of how brain-wide neural connectivity supports and organizes sensory, behavioral, and cognitive processes (3). Recent advances in structural (2, 4) and functional connectivity (5-12) mapping, as well as neural circuit modulatory tools, such as optogenetics (13, 14), permit detailed, high-resolution neural examinations at unprecedented scales. In particular, functional connectivity mapping using resting-state functional MRI (rsfMRI) produces noninvasive visualization of slow and spontaneous hemodynamic fluctuations in humans (5-9) and animals (10-12). Coherent low-frequency (<1 Hz) fluctuations across functionally coupled, large-scale networks is an intriguing property, although the exact underlying neural bases and functional significance remain unclear. Previous studies integrating large-scale electrical recordings, voltage-sensitive dye (VSD), and Ca 2+ -imaging techniques (15-18) support the hypothesis that slow, oscillating neural activity constrains and elicits these hemodynamic fluctuations. Furthermore, low-frequency activity can temporally synchronize remote brain region...

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Section: Discussionmentioning

confidence: 99%

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Leong

Chan

Gao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…It is clear, however, that the integration of weak specific signals from individual sensory systems improves the accuracy and speed of detection (17)(18)(19). To assess multisensory facilitation of sickness-cue detection and its neural correlates, we investigated changes in whole-brain activation in response to the presentation of sick and healthy faces combined with the presentation of body odors of sick and healthy individuals, and we assessed "liking behavior" toward the faces.…”

Section: Significancementioning

confidence: 99%

Behavioral and neural correlates to multisensory detection of sick humans

Regenbogen

Axelsson

Lasselin

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

119

110

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Throughout human evolution, infectious diseases have been a primary cause of death. Detection of subtle cues indicating sickness and avoidance of sick conspecifics would therefore be an adaptive way of coping with an environment fraught with pathogens. This study determines how humans perceive and integrate early cues of sickness in conspecifics sampled just hours after the induction of immune system activation, and the underlying neural mechanisms for this detection. In a double-blind placebo-controlled crossover design, the immune system in 22 sample donors was transiently activated with an endotoxin injection [lipopolysaccharide (LPS)]. Facial photographs and body odor samples were taken from the same donors when "sick" (LPS-injected) and when "healthy" (saline-injected) and subsequently were presented to a separate group of participants (n = 30) who rated their liking of the presented person during fMRI scanning. Faces were less socially desirable when sick, and sick body odors tended to lower liking of the faces. Sickness status presented by odor and facial photograph resulted in increased neural activation of odor-and faceperception networks, respectively. A superadditive effect of olfactory-visual integration of sickness cues was found in the intraparietal sulcus, which was functionally connected to core areas of multisensory integration in the superior temporal sulcus and orbitofrontal cortex. Taken together, the results outline a disease-avoidance model in which neural mechanisms involved in the detection of disease cues and multisensory integration are vital parts.body odor | lipopolysaccharide | endotoxin | sickness cues | disease avoidance

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“…For example, a visual-auditory neuron with a visual receptive field in central space will be responsive to auditory cues in a roughly overlapping region of auditory space. The response of SC neurons to cross-modal stimuli is typically stronger than one evoked by either of the modality-specific stimuli [45].…”

Section: Varieties Of Cross-modal Responsesmentioning

confidence: 99%

“…The hallmark of a conjunctive neuron is that its response to the simultaneous presence of stimuli from different modalities is significantly stronger than its response to either stimulus presented alone (see [45]). In contrast, the maximal response of a disjunctive neuron can be produced by a stimulus from a single modality.…”

Section: Varieties Of Cross-modal Responsesmentioning

confidence: 99%

A Defense of an Amodal Number System

Paz

2018

Philosophies

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It has been argued that the approximate number system (ANS) constitutes a problem for the grounded approach to cognition because it implies that some conceptual tasks are performed by non-perceptual systems. The ANS is considered non-perceptual mainly because it processes stimuli from different modalities. Jones (2015) has recently argued that this system has many features (such as being modular) which are characteristic of sensory systems. Additionally, he affirms that traditional sensory systems also process inputs from different modalities. This suggests that the ANS is a perceptual system and therefore it is not problematic for the grounded view. In this paper, I defend the amodal approach to the ANS against these two arguments. In the first place, perceptual systems do not possess the properties attributed to the ANS and therefore these properties do not imply that the ANS is perceptual. In the second place, I will propose that a sensory system only needs to be dedicated to process modality-specific information, which is consistent with responding to inputs from different modalities. I argue that the cross-modal responses exhibited by traditional sensory systems are consistent with modality-specific information whereas some responses exhibited by the ANS are not.

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Development of multisensory integration from the perspective of the individual neuron

Cited by 329 publications

References 167 publications

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Long-range projections coordinate distributed brain-wide neural activity with a specific spatiotemporal profile

Behavioral and neural correlates to multisensory detection of sick humans

A Defense of an Amodal Number System

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