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Journal of Neuroscience
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Sensory target detection at local and global timescales reveals a hierarchy of supramodal dynamics in the human cortex

Authors: Maria Niedernhuber; Federico Raimondo; Jacobo D. Sitt; Tristan A. Bekinschtein;

Sensory target detection at local and global timescales reveals a hierarchy of supramodal dynamics in the human cortex

Abstract

AbstractTo ensure survival in a dynamic environment, the human neocortex monitors input streams forwarded from different sensory organs for important sensory events. Which principles govern whether different senses share common or modality-specific networks for sensory target detection? We examined whether complex targets evoke sustained supramodal activity while simple targets rely on modality-specific networks with short-lived supramodal contributions. In a series of hierarchical multisensory target detection studies (n=77, of either sex) using Electroencephalography, we applied a temporal cross-decoding approach to dissociate supramodal and modality-specific cortical dynamics elicited by rule-based global and feature-based local sensory deviations within and between the visual, somatosensory and auditory modality. Our data show that each sense implements a cortical hierarchy which orchestrates supramodal target detection responses operating on local and global timescales at successive processing stages. Across different sensory modalities, simple feature-based sensory deviations presented in temporal vicinity to a monotonous input stream triggered an MMN-like local negativity which decayed quickly and early whereas complex rule-based targets tracked across time evoked a P3b-like global ERP response which generalised across a late time window. Converging results from temporal cross-modality decoding analyses across different datasets, we reveal that global ERP responses are sustained in a supramodal higher-order network whereas local ERP responses canonically thought to rely on modality-specific regions evolve into short-lived supramodal activity. Taken together, our findings demonstrate that cortical organisation largely follows a gradient in which short-lived modality-specific as well as supramodal processes dominate local responses whereas higher-order processes encode temporally extended abstract supramodal information fed forward from modality-specific cortices. Sensory target detection at local and global timescales reveals a hierarchy of supramodal dynamics in the human cortexSignificance statementEach sense supports a cortical hierarchy of processes tracking deviant sensory events at multiple timescales. Conflicting evidence produced a lively debate around which of these processes are supramodal. Here, we manipulated the temporal complexity of auditory, tactile, and visual targets to determine whether cortical local and global ERP responses to sensory targets share cortical dynamics between the senses. Using temporal cross-decoding, we found that temporally complex targets elicit a supramodal sustained response. Conversely, local responses to temporally confined targets typically considered modality-specific rely on early short-lived supramodal activation. Our finding provides evidence for a supramodal gradient supporting sensory target detection in the cortex, with implications for multiple fields in which these responses are studied (such as predictive coding, consciousness, and attention).

Keywords

Brain Mapping, multisensory processing, hierarchical predictive coding, target detection, Brain, attention, supramodal processing, Touch Perception, Acoustic Stimulation, Time Perception, Auditory Perception, Humans, Attention, [SDV.NEU] Life Sciences [q-bio]/Neurons and Cognition [q-bio.NC], electroencephalography, info:eu-repo/classification/ddc/610

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    Top 10%
    influence
    This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
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    impulse
    This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
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selected citations
These citations are derived from selected sources.
This is an alternative to the "Influence" indicator, which also reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Citations provided by BIP!
popularity
This indicator reflects the "current" impact/attention (the "hype") of an article in the research community at large, based on the underlying citation network.
BIP!Popularity provided by BIP!
influence
This indicator reflects the overall/total impact of an article in the research community at large, based on the underlying citation network (diachronically).
BIP!Influence provided by BIP!
impulse
This indicator reflects the initial momentum of an article directly after its publication, based on the underlying citation network.
BIP!Impulse provided by BIP!
4
Top 10%
Average
Average
Green
hybrid