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Top-down, contextual entrainment of neuronal oscillations in the auditory thalamocortical circuit.

ABSTRACT: Prior studies have shown that repetitive presentation of acoustic stimuli results in an alignment of ongoing neuronal oscillations to the sequence rhythm via oscillatory entrainment by external cues. Our study aimed to explore the neural correlates of the perceptual parsing and grouping of complex repeating auditory patterns that occur based solely on statistical regularities, or context. Human psychophysical studies suggest that the recognition of novel auditory patterns amid a continuous auditory stimulus sequence occurs automatically halfway through the first repetition. We hypothesized that once repeating patterns were detected by the brain, internal rhythms would become entrained, demarcating the temporal structure of these repetitions despite lacking external cues defining pattern on- or offsets. To examine the neural correlates of pattern perception, neuroelectric activity of primary auditory cortex (A1) and thalamic nuclei was recorded while nonhuman primates passively listened to streams of rapidly presented pure tones and bandpass noise bursts. At arbitrary intervals, random acoustic patterns composed of 11 stimuli were repeated five times without any perturbance of the constant stimulus flow. We found significant delta entrainment by these patterns in the A1, medial geniculate body, and medial pulvinar. In A1 and pulvinar, we observed a statistically significant, pattern structure-aligned modulation of neuronal firing that occurred earliest in the pulvinar, supporting the idea that grouping and detecting complex auditory patterns is a top-down, context-driven process. Besides electrophysiological measures, a pattern-related modulation of pupil diameter verified that, like humans, nonhuman primates consciously detect complex repetitive patterns that lack physical boundaries.

SUBMITTER: Barczak A

PROVIDER: S-EPMC6094129 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Top-down, contextual entrainment of neuronal oscillations in the auditory thalamocortical circuit.

Barczak Annamaria A O'Connell Monica Noelle MN McGinnis Tammy T Ross Deborah D Mowery Todd T Falchier Arnaud A Lakatos Peter P

Proceedings of the National Academy of Sciences of the United States of America 20180723 32

Prior studies have shown that repetitive presentation of acoustic stimuli results in an alignment of ongoing neuronal oscillations to the sequence rhythm via oscillatory entrainment by external cues. Our study aimed to explore the neural correlates of the perceptual parsing and grouping of complex repeating auditory patterns that occur based solely on statistical regularities, or context. Human psychophysical studies suggest that the recognition of novel auditory patterns amid a continuous audit ...[more]

PMID: 30037997

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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, contextual entrainment of neuronal oscillations in the auditory thalamocortical circuit.

Publications

Top-down, contextual entrainment of neuronal oscillations in the auditory thalamocortical circuit.

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