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Neural substrates of reliability-weighted visual-tactile multisensory integration.

Beauchamp MS, Pasalar S, Ro T - Front Syst Neurosci (2010)

Bottom Line: When subjects detected viewed and felt touches to the hand, a network of brain areas was active, including visual areas in lateral occipital cortex, somatosensory areas in inferior parietal lobe, and multisensory areas in the intraparietal sulcus (IPS).In agreement with the weighted connection model, the connection weight measured with structural equation modeling between somatosensory cortex and IPS increased for somatosensory-reliable stimuli, and the connection weight between visual cortex and IPS increased for visual-reliable stimuli.This double dissociation of connection strengths was similar to the pattern of behavioral responses during incongruent multisensory stimulation, suggesting that weighted connections may be a neural mechanism for behavioral reliability weighting.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology and Anatomy, University of Texas Health Science Center at Houston Houston, TX, USA.

ABSTRACT
As sensory systems deteriorate in aging or disease, the brain must relearn the appropriate weights to assign each modality during multisensory integration. Using blood-oxygen level dependent functional magnetic resonance imaging of human subjects, we tested a model for the neural mechanisms of sensory weighting, termed "weighted connections." This model holds that the connection weights between early and late areas vary depending on the reliability of the modality, independent of the level of early sensory cortex activity. When subjects detected viewed and felt touches to the hand, a network of brain areas was active, including visual areas in lateral occipital cortex, somatosensory areas in inferior parietal lobe, and multisensory areas in the intraparietal sulcus (IPS). In agreement with the weighted connection model, the connection weight measured with structural equation modeling between somatosensory cortex and IPS increased for somatosensory-reliable stimuli, and the connection weight between visual cortex and IPS increased for visual-reliable stimuli. This double dissociation of connection strengths was similar to the pattern of behavioral responses during incongruent multisensory stimulation, suggesting that weighted connections may be a neural mechanism for behavioral reliability weighting.

No MeSH data available.


Related in: MedlinePlus

Summary of fMRI activations. (A) Activation during performance of the multisensory touch detection task shown on an inflated average cortical surface model (left hemisphere, single subject). The orange circle highlights active visual areas in lateral occipital cortex. The blue circle highlights active areas in inferior parietal lobe, the location of secondary somatosensory cortex. The green circle highlights active areas in and around the intraparietal sulcus (IPS). The horizontal dashed white line shows the intraparietal sulcus, vertical dashed white line shows the postcentral sulcus. (B) Group activation map from n = 8 subjects. (C) Time course of the BOLD response in the visual cortex ROI during 20 s stimulation blocks of each experimental condition, averaged across blocks and subjects (black lines show the mean percent signal change, gray lines show + -SEM). (D) Time course of the somatosensory cortex response. (E) Time course of the IPS response.
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Figure 3: Summary of fMRI activations. (A) Activation during performance of the multisensory touch detection task shown on an inflated average cortical surface model (left hemisphere, single subject). The orange circle highlights active visual areas in lateral occipital cortex. The blue circle highlights active areas in inferior parietal lobe, the location of secondary somatosensory cortex. The green circle highlights active areas in and around the intraparietal sulcus (IPS). The horizontal dashed white line shows the intraparietal sulcus, vertical dashed white line shows the postcentral sulcus. (B) Group activation map from n = 8 subjects. (C) Time course of the BOLD response in the visual cortex ROI during 20 s stimulation blocks of each experimental condition, averaged across blocks and subjects (black lines show the mean percent signal change, gray lines show + -SEM). (D) Time course of the somatosensory cortex response. (E) Time course of the IPS response.

Mentions: When subjects viewed and felt touches, the largest clusters of activity were observed in extrastriate visual areas in lateral occipital cortex, in inferior parietal lobe in the location of secondary somatosensory cortex and associated areas, and in anterior IPS near the junction with postcentral sulcus (see Figure 3 and Table 1 for a list of all active regions). We measured BOLD fMRI activity in three regions of interest (visual, somatosensory, and IPS) in order to test the two competing models of multisensory integration (see Figure 3 for the average time series from each ROI for each stimulus condition). As shown in Figure 4, the response to unreliable stimuli was slightly greater than the response to reliable stimuli (0.92% vs. 0.76% for somatosensory, 2.7% vs. 2.3% for visual, p = 0.06 in a paired t-test). We examined the connectivity between visual cortex, somatosensory cortex and IPS during presentation of multisensory stimuli with varying stimulus reliability (Figure 5). The connection weight, measured as a correlation coefficient, between somatosensory cortex and IPS was lower during somatosensory-unreliable stimulation than during somatosensory-reliable stimulation (0.24 vs. 0.38, p = 0.002 in a paired t-test), even though somatosensory cortex was slightly more activated in the unreliable condition. Similarly, the connection weight between visual cortex and IPS was lower during visual-unreliable stimulation than during visual-reliable stimulation (0.23 vs. 0.32, p = 0.001), even though visual cortex was slightly more activated in the unreliable condition. As predicted by the weighted connections model, the connection weights were higher for the reliable stimulus modality despite there being less activity in the unisensory cortices for the reliable as compared to the unreliable conditions. The connection weight changes (higher for reliable stimuli) were in the opposite direction as the mean BOLD signal change (lower for reliable stimuli). The connection weight between visual cortex and somatosensory cortex was unaffected by reliability (0.11 vs. 0.15, p = 0.3).


Neural substrates of reliability-weighted visual-tactile multisensory integration.

Beauchamp MS, Pasalar S, Ro T - Front Syst Neurosci (2010)

Summary of fMRI activations. (A) Activation during performance of the multisensory touch detection task shown on an inflated average cortical surface model (left hemisphere, single subject). The orange circle highlights active visual areas in lateral occipital cortex. The blue circle highlights active areas in inferior parietal lobe, the location of secondary somatosensory cortex. The green circle highlights active areas in and around the intraparietal sulcus (IPS). The horizontal dashed white line shows the intraparietal sulcus, vertical dashed white line shows the postcentral sulcus. (B) Group activation map from n = 8 subjects. (C) Time course of the BOLD response in the visual cortex ROI during 20 s stimulation blocks of each experimental condition, averaged across blocks and subjects (black lines show the mean percent signal change, gray lines show + -SEM). (D) Time course of the somatosensory cortex response. (E) Time course of the IPS response.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC2903191&req=5

Figure 3: Summary of fMRI activations. (A) Activation during performance of the multisensory touch detection task shown on an inflated average cortical surface model (left hemisphere, single subject). The orange circle highlights active visual areas in lateral occipital cortex. The blue circle highlights active areas in inferior parietal lobe, the location of secondary somatosensory cortex. The green circle highlights active areas in and around the intraparietal sulcus (IPS). The horizontal dashed white line shows the intraparietal sulcus, vertical dashed white line shows the postcentral sulcus. (B) Group activation map from n = 8 subjects. (C) Time course of the BOLD response in the visual cortex ROI during 20 s stimulation blocks of each experimental condition, averaged across blocks and subjects (black lines show the mean percent signal change, gray lines show + -SEM). (D) Time course of the somatosensory cortex response. (E) Time course of the IPS response.
Mentions: When subjects viewed and felt touches, the largest clusters of activity were observed in extrastriate visual areas in lateral occipital cortex, in inferior parietal lobe in the location of secondary somatosensory cortex and associated areas, and in anterior IPS near the junction with postcentral sulcus (see Figure 3 and Table 1 for a list of all active regions). We measured BOLD fMRI activity in three regions of interest (visual, somatosensory, and IPS) in order to test the two competing models of multisensory integration (see Figure 3 for the average time series from each ROI for each stimulus condition). As shown in Figure 4, the response to unreliable stimuli was slightly greater than the response to reliable stimuli (0.92% vs. 0.76% for somatosensory, 2.7% vs. 2.3% for visual, p = 0.06 in a paired t-test). We examined the connectivity between visual cortex, somatosensory cortex and IPS during presentation of multisensory stimuli with varying stimulus reliability (Figure 5). The connection weight, measured as a correlation coefficient, between somatosensory cortex and IPS was lower during somatosensory-unreliable stimulation than during somatosensory-reliable stimulation (0.24 vs. 0.38, p = 0.002 in a paired t-test), even though somatosensory cortex was slightly more activated in the unreliable condition. Similarly, the connection weight between visual cortex and IPS was lower during visual-unreliable stimulation than during visual-reliable stimulation (0.23 vs. 0.32, p = 0.001), even though visual cortex was slightly more activated in the unreliable condition. As predicted by the weighted connections model, the connection weights were higher for the reliable stimulus modality despite there being less activity in the unisensory cortices for the reliable as compared to the unreliable conditions. The connection weight changes (higher for reliable stimuli) were in the opposite direction as the mean BOLD signal change (lower for reliable stimuli). The connection weight between visual cortex and somatosensory cortex was unaffected by reliability (0.11 vs. 0.15, p = 0.3).

Bottom Line: When subjects detected viewed and felt touches to the hand, a network of brain areas was active, including visual areas in lateral occipital cortex, somatosensory areas in inferior parietal lobe, and multisensory areas in the intraparietal sulcus (IPS).In agreement with the weighted connection model, the connection weight measured with structural equation modeling between somatosensory cortex and IPS increased for somatosensory-reliable stimuli, and the connection weight between visual cortex and IPS increased for visual-reliable stimuli.This double dissociation of connection strengths was similar to the pattern of behavioral responses during incongruent multisensory stimulation, suggesting that weighted connections may be a neural mechanism for behavioral reliability weighting.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurobiology and Anatomy, University of Texas Health Science Center at Houston Houston, TX, USA.

ABSTRACT
As sensory systems deteriorate in aging or disease, the brain must relearn the appropriate weights to assign each modality during multisensory integration. Using blood-oxygen level dependent functional magnetic resonance imaging of human subjects, we tested a model for the neural mechanisms of sensory weighting, termed "weighted connections." This model holds that the connection weights between early and late areas vary depending on the reliability of the modality, independent of the level of early sensory cortex activity. When subjects detected viewed and felt touches to the hand, a network of brain areas was active, including visual areas in lateral occipital cortex, somatosensory areas in inferior parietal lobe, and multisensory areas in the intraparietal sulcus (IPS). In agreement with the weighted connection model, the connection weight measured with structural equation modeling between somatosensory cortex and IPS increased for somatosensory-reliable stimuli, and the connection weight between visual cortex and IPS increased for visual-reliable stimuli. This double dissociation of connection strengths was similar to the pattern of behavioral responses during incongruent multisensory stimulation, suggesting that weighted connections may be a neural mechanism for behavioral reliability weighting.

No MeSH data available.


Related in: MedlinePlus