Attention modulates topology and dynamics of auditory sensory gating

Abstract

This work challenges the widely accepted model of sensory gating as a preattention inhibitory process by investigating whether attention directed at the second tone (S2) within a paired‐click paradigm could affect gating at the cortical level. We utilized magnetoencephalography, magnetic resonance imaging and spatio‐temporal source localization to compare the cortical dynamics underlying gating responses across two conditions (passive and attention) in 19 healthy subjects. Source localization results reaffirmed the existence of a fast processing pathway between the prefrontal cortex (PFC) and bilateral superior temporal gyri (STG) that underlies the auditory gating process. STG source dynamics comprised two gating sub‐components, Mb1 and Mb2, both of which showed significant gating suppression (>51%). The attention directed to the S2 tone changed the gating network topology by switching the prefrontal generator from a dorsolateral location, which was active in the passive condition (18/19), to a medial location, active in the attention condition (19/19). Enhanced responses to the attended stimulus caused a significant reduction in gating suppression in both STG gating components (>50%). Our results demonstrate that attention not only modulates sensory gating dynamics, but also exerts topological rerouting of information processing within the PFC. The present data, suggesting that the cortical levels of early sensory processing are subject to top‐down influences, change the current view of gating as a purely automatic bottom‐up process.

Topological Biomarker of Alzheimer’s Disease

“…Our novel research provides evidence that passive paired-click and oddball paradigms activate a different prefrontal generator within the auditory gating network [60,96]. Spatiotemporal source localization of auditory gating responses evoked by the passive paired-click paradigm revealed a different gating topology consisting of a dorsolateral PFC (dlPFC) source in addition to the sources in the bilateral primary auditory cortices [78,96], as shown in panel B) of Figure 1.…”

“…Our novel research provides evidence that passive paired-click and oddball paradigms activate a different prefrontal generator within the auditory gating network [60,96]. Spatiotemporal source localization of auditory gating responses evoked by the passive paired-click paradigm revealed a different gating topology consisting of a dorsolateral PFC (dlPFC) source in addition to the sources in the bilateral primary auditory cortices [78,96], as shown in panel B) of Figure 1. This result implies the existence of early rerouting within prefrontal cortex by shifting prefrontal gating activation from dorsolateral to medial prefrontal region, depending on a paradigm [60,96], suggesting that mPFC and dlPFC regions serve different functions involved during the early sensory processing.…”

“…Using the oddball paradigm, which evokes both gating-in and gating-out mechanisms, we have demonstrated that auditory gating network comprises a medial prefrontal (mPFC) generator along with the anticipated generators in the bilateral primary auditory cortices [60,64,96], as shown in panel A) of Figure 1. Our finding suggests the existence of a novel, very fast sensory processing stream (i.e., sensory gating loop), which links executive PFC to primary auditory cortex within the first 50 ms after stimulus presentation, alongside well-affirmed but slower limbic (dorsal) and somatic (ventral) sensory processing pathways [60,96]. The existence of additional fast sensory processing stream, sensory gating loop, is anatomically supported by dense bidirectional connections between medial PFC and superior temporal cortices found in both primate and human anatomical studies [97,98].…”

“…Efforts to delineate the neuroanatomy of the sensory gating network long have yielded inconsistent findings [90][91][92][93]. The recent works, relied on advanced MEG-based multi-dipole source localization, finally provide a reliable set of neural generators [60,64,[94][95][96]. Moreover, our novel results revealed possible explanations concerning the problem of inconsistent reports regarding auditory gating network topology, suggesting that paired-click and oddball paradigms, which are often used to challenge sensory gating effects, evoke different gating generator topologies, even though they are both passive for the subjects [96].…”

“…Spatiotemporal source localization of auditory gating responses evoked by the passive paired-click paradigm revealed a different gating topology consisting of a dorsolateral PFC (dlPFC) source in addition to the sources in the bilateral primary auditory cortices [78,96], as shown in panel B) of Figure 1. This result implies the existence of early rerouting within prefrontal cortex by shifting prefrontal gating activation from dorsolateral to medial prefrontal region, depending on a paradigm [60,96], suggesting that mPFC and dlPFC regions serve different functions involved during the early sensory processing. A passive paired-click paradigm characterized Topological Biomarker of Alzheimer's Disease http://dx.doi.org/10.5772/intechopen.76633 by the constant repetition of both short-and long-term patterns (S1-500 ms; S2-8 s) could result in long-term repetition suppression produced by the dlPFC.…”