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Fear learning enhances neural responses to threat-predictive sensory stimuli.

ABSTRACT: The central nervous system rapidly learns that particular stimuli predict imminent danger. This learning is thought to involve associations between neutral and harmful stimuli in cortical and limbic brain regions, though associative neuroplasticity in sensory structures is increasingly appreciated. We observed the synaptic output of olfactory sensory neurons (OSNs) in individual mice before and after they learned that a particular odor indicated an impending foot shock. OSNs are the first cells in the olfactory system, physically contacting the odor molecules in the nose and projecting their axons to the brain's olfactory bulb. OSN output evoked by the shock-predictive odor was selectively facilitated after fear conditioning. These results indicate that affective information about a stimulus can be encoded in its very earliest representation in the nervous system.

SUBMITTER: Kass MD

PROVIDER: S-EPMC4011636 | biostudies-literature | 2013 Dec

REPOSITORIES: biostudies-literature

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Fear learning enhances neural responses to threat-predictive sensory stimuli.

Kass Marley D MD Rosenthal Michelle C MC Pottackal Joseph J McGann John P JP

Science (New York, N.Y.) 20131201 6164

The central nervous system rapidly learns that particular stimuli predict imminent danger. This learning is thought to involve associations between neutral and harmful stimuli in cortical and limbic brain regions, though associative neuroplasticity in sensory structures is increasingly appreciated. We observed the synaptic output of olfactory sensory neurons (OSNs) in individual mice before and after they learned that a particular odor indicated an impending foot shock. OSNs are the first cells ...[more]

PMID: 24337299

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Project description:Contextual information triggers predictions about the content ("what") of environmental stimuli to update an internal generative model of the surrounding world. However, visual information dynamically changes across time, and temporal predictability ("when") may influence the impact of internal predictions on visual processing. In this magnetoencephalography (MEG) study, we investigated how processing feature specific information ("what") is affected by temporal predictability ("when"). Participants (N = 16) were presented with four consecutive Gabor patches (entrainers) with constant spatial frequency but with variable orientation and temporal onset. A fifth target Gabor was presented after a longer delay and with higher or lower spatial frequency that participants had to judge. We compared the neural responses to entrainers where the Gabor orientation could, or could not be temporally predicted along the entrainer sequence, and with inter-entrainer timing that was constant (predictable), or variable (unpredictable). We observed suppression of evoked neural responses in the visual cortex for predictable stimuli. Interestingly, we found that temporal uncertainty increased expectation suppression. This suggests that in temporally uncertain scenarios the neurocognitive system invests less resources in integrating bottom-up information. Multivariate pattern analysis showed that predictable visual features could be decoded from neural responses. Temporal uncertainty did not affect decoding accuracy for early visual responses, with the feature specificity of early visual neural activity preserved across conditions. However, decoding accuracy was less sustained over time for temporally jittered than for isochronous predictable visual stimuli. These findings converge to suggest that the cognitive system processes visual features of temporally predictable stimuli in higher detail, while processing temporally uncertain stimuli may rely more heavily on abstract internal expectations.

Dataset Information

Fear learning enhances neural responses to threat-predictive sensory stimuli.

Publications

Fear learning enhances neural responses to threat-predictive sensory stimuli.

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