Dataset Information

Top-down attention switches coupling between low-level and high-level areas of human visual cortex.

ABSTRACT: Top-down attention is an essential cognitive ability, allowing our finite brains to process complex natural environments by prioritizing information relevant to our goals. Previous evidence suggests that top-down attention operates by modulating stimulus-evoked neural activity within visual areas specialized for processing goal-relevant information. We show that top-down attention also has a separate influence on the background coupling between visual areas: adopting different attentional goals resulted in specific patterns of noise correlations in the visual system, whereby intrinsic activity in the same set of low-level areas was shared with only those high-level areas relevant to the current goal. These changes occurred independently of evoked activity, persisted without visual stimulation, and predicted behavioral success in deploying attention better than the modulation of evoked activity. This attentional switching of background connectivity suggests that attention may help synchronize different levels of the visual processing hierarchy, forming state-dependent functional pathways in human visual cortex to prioritize goal-relevant information.

SUBMITTER: Al-Aidroos N

PROVIDER: S-EPMC3437858 | biostudies-literature | 2012 Sep

REPOSITORIES: biostudies-literature

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Top-down attention switches coupling between low-level and high-level areas of human visual cortex.

Al-Aidroos Naseem N Said Christopher P CP Turk-Browne Nicholas B NB

Proceedings of the National Academy of Sciences of the United States of America 20120820 36

Top-down attention is an essential cognitive ability, allowing our finite brains to process complex natural environments by prioritizing information relevant to our goals. Previous evidence suggests that top-down attention operates by modulating stimulus-evoked neural activity within visual areas specialized for processing goal-relevant information. We show that top-down attention also has a separate influence on the background coupling between visual areas: adopting different attentional goals ...[more]

PMID: 22908274

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Project description:Unified visual perception relies on the integration of bottom-up and top-down inputs in the primary visual cortex (V1), with top-down inputs known to provide behavior-related modulation on visual processing. However, the organization of top-down inputs in V1 remains unclear. Here, using optogenetics-assisted circuit mapping, we characterized how multiple top-down inputs from higher-order cortical and thalamic areas engage excitatory and inhibitory neurons in V1. Systematic layer- and cell-type-specific profiling of the innervation properties of top-down inputs ultimately revealed that each top-down input employs a unique laminar profile when innervating V1. These profiles partially overlap in superficial layers, bypass layer 4 (L4), and clearly segregate upon reaching deep layers. Specifically, inputs from the medial secondary visual cortex (V2M) and anterior cingulate cortex (ACA) preferentially activate L6 neurons, while inputs from the ventrolateral orbitofrontal cortex (ORBvl) and lateral posterior thalamic nucleus (LP) activate L5 neurons. Having defined the inputs, we conducted independent optogenetic activation studies and discovered that ORBvl and LP inputs selectively activate two types of pyramidal neurons (Pyrs) in L5: Pyr <-- ORBvl and Pyr <-- LP neurons, each with specific electrophysiological properties and gene expression profiles. Retrograde mapping subsequently revealed that Pyr <-- ORBvl neurons preferentially innervate subcortical areas and Pyr <-- LP neurons innervate cortical areas, indicating parallel processing of ORBvl and LP inputs in Pyr-type-specific subnetworks. Further, we found mutual inhibition between these two subnetworks, as LP inputs indirectly inhibit Pyr <-- ORBvl neurons and ORBvl inputs inhibit Pyr <-- LP neurons through local inhibitory neurons. Our study thus deepens understanding of the neuronal mechanisms involved in top-down modulation of visual processing by providing a valuable resource characterizing the layer- and cell-type-specific organization of top-down inputs in V1 and by revealing that L5 Pyr-type-specific subnetworks engage in parallel processing of corticocortical and thalamocortical top-down inputs.

Dataset Information

Top-down attention switches coupling between low-level and high-level areas of human visual cortex.

Publications

Top-down attention switches coupling between low-level and high-level areas of human visual cortex.

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