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The prelimbic cortex regulates itch processing by controlling attentional bias.

ABSTRACT: Itch is a complex and unpleasant sensory experience. Recent studies have begun to investigate the neural mechanisms underlying the modulation of sensory and emotional components of itch in the brain. However, the key brain regions and neural mechanism involved in modulating the attentional processing of itch remain elusive. Here, we showed that the prelimbic cortex (PrL) is associated with itch processing and that the manipulation of itch-responsive neurons in the PrL significantly disrupted itch-induced scratching. Interestingly, we found that increasing attentional bias toward a distracting stimulus could disturb itch processing. We also demonstrated the existence of a population of attention-related neurons in the PrL that drive attentional bias to regulate itch processing. Importantly, itch-responsive neurons and attention-related neurons significantly overlapped in the PrL and were mutually interchangeable in the regulation of itch processing at the cellular activity level. Our results revealed that the PrL regulates itch processing by controlling attentional bias.

SUBMITTER: Wu GY

PROVIDER: S-EPMC9816985 | biostudies-literature | 2023 Jan

REPOSITORIES: biostudies-literature

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The prelimbic cortex regulates itch processing by controlling attentional bias.

Wu Guang-Yan GY Zheng Xiao-Xia XX Zhao Shan-Lan SL Wang Yi Y Jiang Shan S Wang Yi-Song YS Yi Yi-Lun YL Yao Juan J Wen Hui-Zhong HZ Liu Ju J Li Hong-Li HL Sui Jian-Feng JF

iScience 20221217 1

Itch is a complex and unpleasant sensory experience. Recent studies have begun to investigate the neural mechanisms underlying the modulation of sensory and emotional components of itch in the brain. However, the key brain regions and neural mechanism involved in modulating the attentional processing of itch remain elusive. Here, we showed that the prelimbic cortex (PrL) is associated with itch processing and that the manipulation of itch-responsive neurons in the PrL significantly disrupted itc ...[more]

PMID: 36619983

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Project description:Sustained attention, the ability to focus on a stimulus or task over extended periods, is crucial for higher level cognition, and is impaired in individuals diagnosed with neuropsychiatric and neurodevelopmental disorders, including attention-deficit/hyperactivity disorder, schizophrenia, and depression. Translational tasks like the rodent continuous performance test (rCPT) can be used to study the cellular mechanisms underlying sustained attention. Accumulating evidence points to a role for the prelimbic cortex (PrL) in sustained attention, as electrophysiological single unit and local field (LFPs) recordings reflect changes in neural activity in the PrL in mice performing sustained attention tasks. While the evidence correlating PrL electrical activity with sustained attention is compelling, limitations inherent to electrophysiological recording techniques, including low sampling in single unit recordings and source ambivalence for LFPs, impede the ability to fully resolve the cellular mechanisms in the PrL that contribute to sustained attention. In vivo endoscopic calcium imaging using genetically encoded calcium sensors in behaving animals can address these questions by simultaneously recording up to hundreds of neurons at single cell resolution. Here, we used in vivo endoscopic calcium imaging to record patterns of neuronal activity in PrL neurons using the genetically encoded calcium sensor GCaMP6f in mice performing the rCPT at three timepoints requiring differing levels of cognitive demand and task proficiency. A higher proportion of PrL neurons were recruited during correct responses in sessions requiring high cognitive demand and task proficiency, and mice intercalated non-responsive-disengaged periods with responsive-engaged periods that resemble attention lapses. During disengaged periods, the correlation of calcium activity between PrL neurons was higher compared to engaged periods, suggesting a neuronal network state change during attention lapses in the PrL. Overall, these findings illustrate that cognitive demand, task proficiency, and task engagement differentially recruit activity in a subset of PrL neurons during sustained attention.

Project description:Threatening stimuli seem to capture attention more swiftly than neutral stimuli. This attention bias has been observed under different experimental conditions and with different types of stimuli. It remains unclear whether this adaptive behaviour reflects the function of automatic or controlled attention mechanisms. Additionally, the spatiotemporal dynamics of its neural correlates are largely unknown. The present study investigates these issues using an Emotional Flanker Task synchronized with EEG recordings. A group of 32 healthy participants saw response-relevant images (emotional scenes from IAPS or line drawings of objects) flanked by response-irrelevant distracters (i.e., emotional scenes flanked by line drawings or vice versa). We assessed behavioural and ERP responses drawn from four task conditions (Threat-Central, Neutral-Central, Threat-Peripheral, and Neutral-Peripheral) and subjected these responses to repeated-measures ANOVA models. When presented as response-relevant targets, threatening images attracted faster and more accurate responses. They did not affect response accuracy to targets when presented as response-irrelevant flankers. However, response times were significantly slower when threatening images flanked objects than when neutral images were shown as flankers. This result replicated the well-known Emotional Flanker Effect. Behavioural responses to response-relevant threatening targets were accompanied by significant modulations of ERP activity across all time-windows and regions of interest and displayed some meaningful correlations. The Emotional Flanker Effect was accompanied by a modulation over parietal and central-parietal regions within a time-window between 550-690ms. Such a modulation suggests that the attentional disruption to targets caused by response-irrelevant threatening flankers appears to reflect less neural resources available, which are seemingly drawn away by distracting threatening flankers. The observed spatiotemporal dynamics seem to concur with understanding of the important adaptive role attributed to threat-related attention bias.

Dataset Information

The prelimbic cortex regulates itch processing by controlling attentional bias.

Publications

The prelimbic cortex regulates itch processing by controlling attentional bias.

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