It has been postulated that the brain is organized by “metamodal,” sensory-independent cortical modules capable of performing tasks (e.g., word recognition) in both “standard” and novel sensory modalities. Still, this theory has primarily been tested in sensory-deprived individuals, with mixed evidence in neurotypical subjects, thereby limiting its support as a general principle of brain organization. Critically, current theories of metamodal processing do not specify requirements for successful metamodal processing at the level of neural representations. Specification at this level may be particularly important in neurotypical individuals, where novel sensory modalities must interface with existing representations for the standard sense. Here we hypothesized that effective metamodal engagement of a cortical area requires congruence between stimulus representations in the standard and novel sensory modalities in that region. To test this, we first used fMRI to identify bilateral auditory speech representations. We then trained 20 human participants (12 female) to recognize vibrotactile versions of auditory words using one of two auditory-to-vibrotactile algorithms. The vocoded algorithm attempted to match the encoding scheme of auditory speech while the token-based algorithm did not. Crucially, using fMRI, we found that only in the vocoded group did trained-vibrotactile stimuli recruit speech representations in the superior temporal gyrus and lead to increased coupling between them and somatosensory areas. Our results advance our understanding of brain organization by providing new insight into unlocking the metamodal potential of the brain, thereby benefitting the design of novel sensory substitution devices that aim to tap into existing processing streams in the brain.
The grouping of sensory stimuli into categories is fundamental to cognition. Previous research in the visual and auditory systems supports a two‐stage processing hierarchy that underlies perceptual categorization: (a) a “bottom‐up” perceptual stage in sensory cortices where neurons show selectivity for stimulus features and (b) a “top‐down” second stage in higher level cortical areas that categorizes the stimulus‐selective input from the first stage. In order to test the hypothesis that the two‐stage model applies to the somatosensory system, 14 human participants were trained to categorize vibrotactile stimuli presented to their right forearm. Then, during an fMRI scan, participants actively categorized the stimuli. Representational similarity analysis revealed stimulus selectivity in areas including the left precentral and postcentral gyri, the supramarginal gyrus, and the posterior middle temporal gyrus. Crucially, we identified a single category‐selective region in the left ventral precentral gyrus. Furthermore, an estimation of directed functional connectivity delivered evidence for robust top‐down connectivity from the second to first stage. These results support the validity of the two‐stage model of perceptual categorization for the somatosensory system, suggesting common computational principles and a unified theory of perceptual categorization across the visual, auditory, and somatosensory systems.
more » « less- NSF-PAR ID:
- 10461564
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- Human Brain Mapping
- Volume:
- 40
- Issue:
- 10
- ISSN:
- 1065-9471
- Page Range / eLocation ID:
- p. 3078-3090
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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SIGNIFICANCE STATEMENT It has been proposed that the brain is organized by “metamodal,” sensory-independent modules specialized for performing certain tasks. This idea has inspired therapeutic applications, such as sensory substitution devices, for example, enabling blind individuals “to see” by transforming visual input into soundscapes. Yet, other studies have failed to demonstrate metamodal engagement. Here, we tested the hypothesis that metamodal engagement in neurotypical individuals requires matching the encoding schemes between stimuli from the novel and standard sensory modalities. We trained two groups of subjects to recognize words generated by one of two auditory-to-vibrotactile transformations. Critically, only vibrotactile stimuli that were matched to the neural encoding of auditory speech engaged auditory speech areas after training. This suggests that matching encoding schemes is critical to unlocking the brain's metamodal potential. -
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