Dataset Information

Differential Impact of Acute and Chronic Stress on CA1 Spatial Coding and Gamma Oscillations.

ABSTRACT: Chronic and acute stress differentially affect behavior as well as the structural integrity of the hippocampus, a key brain region involved in cognition and memory. However, it remains unclear if and how the facilitatory effects of acute stress on hippocampal information coding are disrupted as the stress becomes chronic. To examine this, we compared the impact of acute and chronic stress on neural activity in the CA1 subregion of male mice subjected to a chronic immobilization stress (CIS) paradigm. We observed that following first exposure to stress (acute stress), the spatial information encoded in the hippocampus sharpened, and the neurons became increasingly tuned to the underlying theta oscillations in the local field potential (LFP). However, following repeated exposure to the same stress (chronic stress), spatial tuning was poorer and the power of both the slow-gamma (30-50 Hz) and fast-gamma (55-90 Hz) oscillations, which correlate with excitatory inputs into the region, decreased. These results support the idea that acute and chronic stress differentially affect neural computations carried out by hippocampal circuits and suggest that acute stress may improve cognitive processing.

SUBMITTER: Tomar A

PROVIDER: S-EPMC8329706 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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Differential Impact of Acute and Chronic Stress on CA1 Spatial Coding and Gamma Oscillations.

Tomar Anupratap A Polygalov Denis D McHugh Thomas J TJ

Frontiers in behavioral neuroscience 20210720

Chronic and acute stress differentially affect behavior as well as the structural integrity of the hippocampus, a key brain region involved in cognition and memory. However, it remains unclear if and how the facilitatory effects of acute stress on hippocampal information coding are disrupted as the stress becomes chronic. To examine this, we compared the impact of acute and chronic stress on neural activity in the CA1 subregion of male mice subjected to a chronic immobilization stress (CIS) para ...[more]

PMID: 34354574

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Project description:Fine-scale temporal organization of cortical activity in the gamma range (∼25-80Hz) may play a significant role in information processing, for example by neural grouping ('binding') and phase coding. Recent experimental studies have shown that the precise frequency of gamma oscillations varies with input drive (e.g. visual contrast) and that it can differ among nearby cortical locations. This has challenged theories assuming widespread gamma synchronization at a fixed common frequency. In the present study, we investigated which principles govern gamma synchronization in the presence of input-dependent frequency modulations and whether they are detrimental for meaningful input-dependent gamma-mediated temporal organization. To this aim, we constructed a biophysically realistic excitatory-inhibitory network able to express different oscillation frequencies at nearby spatial locations. Similarly to cortical networks, the model was topographically organized with spatially local connectivity and spatially-varying input drive. We analyzed gamma synchronization with respect to phase-locking, phase-relations and frequency differences, and quantified the stimulus-related information represented by gamma phase and frequency. By stepwise simplification of our models, we found that the gamma-mediated temporal organization could be reduced to basic synchronization principles of weakly coupled oscillators, where input drive determines the intrinsic (natural) frequency of oscillators. The gamma phase-locking, the precise phase relation and the emergent (measurable) frequencies were determined by two principal factors: the detuning (intrinsic frequency difference, i.e. local input difference) and the coupling strength. In addition to frequency coding, gamma phase contained complementary stimulus information. Crucially, the phase code reflected input differences, but not the absolute input level. This property of relative input-to-phase conversion, contrasting with latency codes or slower oscillation phase codes, may resolve conflicting experimental observations on gamma phase coding. Our modeling results offer clear testable experimental predictions. We conclude that input-dependency of gamma frequencies could be essential rather than detrimental for meaningful gamma-mediated temporal organization of cortical activity.

Project description:Using intracranial electrocorticography, we determined how cortical gamma-oscillations (50-150 Hz) were induced by different visual tasks in nine children with focal epilepsy. In all children, full-field stroboscopic flash-stimuli induced gamma-augmentation in the anterior-medial occipital cortex (starting on average at 31 ms after stimulus presentation) and subsequently in the lateral-polar occipital cortex; minimal gamma-augmentation was noted in the inferior occipital-temporal cortex; occipital gamma-augmentation was followed by gamma-attenuation in three children. Central-field picture-stimuli induced sustained gamma-augmentation in the lateral-polar occipital cortex (starting on average at 69 ms) and subsequently in the inferior occipital-temporal cortex in all children and in the posterior frontal cortex in three children; the anterior-medial occipital cortex showed no gamma-augmentation but rather gamma-attenuation. Electrical stimulation of the anterior-medial occipital cortex induced a phosphene in the peripheral-field or eye deviation to the contralateral side, whereas that of the lateral-polar occipital cortex induced a phosphene in the central-field. In summary, full-field, simple and short-lasting visual information might be preferentially processed by the anterior-medial occipital cortex, and subsequently by the lateral-polar occipital cortex. Gamma-attenuation following augmentation in the striate cortex might be associated with a relative refractory-period to flash-stimuli or feed-forward inhibition by other areas. Central-field complex visual information might be processed by a network involving the lateral-polar occipital cortex and the inferior occipital-temporal cortex. A plausible interpretation of posterior frontal gamma-augmentation during central-field picture stimuli includes activation of the frontal-eye-field for visual searching. Gamma-attenuation in the anterior-medial occipital cortex during central-field picture-stimuli might be associated with relative inattention to the peripheral visual field during central-field object visualization.

Dataset Information

Differential Impact of Acute and Chronic Stress on CA1 Spatial Coding and Gamma Oscillations.

Publications

Differential Impact of Acute and Chronic Stress on CA1 Spatial Coding and Gamma Oscillations.

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