Odor fear conditioning modifies piriform cortex local field potentials both during conditioning and during post-conditioning sleep

Dylan C. Barnes, Julie Chapuis, Dipesh Chaudhury, Donald A. Wilson

    Research output: Contribution to journalArticle

    Abstract

    Background: Sleep plays an active role in memory consolidation. Sleep structure (REM/Slow wave activity [SWS]) can be modified after learning, and in some cortical circuits, sleep is associated with replay of the learned experience. While the majority of this work has focused on neocortical and hippocampal circuits, the olfactory system may offer unique advantages as a model system for exploring sleep and memory, given the short, non-thalamic pathway from nose to primary olfactory (piriform cortex), and rapid cortex-dependent odor learning. Methodology/Principal Findings: We examined piriform cortical odor responses using local field potentials (LFPs) from freely behaving Long-Evans hooded rats over the sleep-wake cycle, and the neuronal modifications that occurred within the piriform cortex both during and after odor-fear conditioning. We also recorded LFPs from naïve animals to characterize sleep activity in the piriform cortex and to analyze transient odor-evoked cortical responses during different sleep stages. Naïve rats in their home cages spent 40% of their time in SWS, during which the piriform cortex was significantly hypo-responsive to odor stimulation compared to awake and REM sleep states. Rats trained in the paired odor-shock conditioning paradigm developed enhanced conditioned odor evoked gamma frequency activity in the piriform cortex over the course of training compared to pseudo-conditioned rats. Furthermore, conditioned rats spent significantly more time in SWS immediately post-training both compared to pre-training days and compared to pseudo-conditioned rats. The increase in SWS immediately after training significantly correlated with the duration of odor-evoked freezing the following day. Conclusions/Significance: The rat piriform cortex is hypo-responsive to odors during SWS which accounts for nearly 40% of each 24 hour period. The duration of slow-wave activity in the piriform cortex is enhanced immediately post-conditioning, and this increase is significantly correlated with subsequent memory performance. Together, these results suggest the piriform cortex may go offline during SWS to facilitate consolidation of learned odors with reduced external interference.

    Original languageEnglish (US)
    Article numbere18130
    JournalPLoS One
    Volume6
    Issue number3
    DOIs
    StatePublished - Mar 28 2011

    Fingerprint

    conditioned behavior
    Odors
    sleep
    fearfulness
    Fear
    cortex
    Sleep
    odors
    Rats
    rats
    REM Sleep
    Data storage equipment
    Consolidation
    learning
    Odorants
    Piriform Cortex
    Conditioning (Psychology)
    Learning
    Slow wave structures
    Long Evans Rats

    ASJC Scopus subject areas

    • Agricultural and Biological Sciences(all)
    • Biochemistry, Genetics and Molecular Biology(all)
    • Medicine(all)

    Cite this

    Odor fear conditioning modifies piriform cortex local field potentials both during conditioning and during post-conditioning sleep. / Barnes, Dylan C.; Chapuis, Julie; Chaudhury, Dipesh; Wilson, Donald A.

    In: PLoS One, Vol. 6, No. 3, e18130, 28.03.2011.

    Research output: Contribution to journalArticle

    Barnes, Dylan C. ; Chapuis, Julie ; Chaudhury, Dipesh ; Wilson, Donald A. / Odor fear conditioning modifies piriform cortex local field potentials both during conditioning and during post-conditioning sleep. In: PLoS One. 2011 ; Vol. 6, No. 3.
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    abstract = "Background: Sleep plays an active role in memory consolidation. Sleep structure (REM/Slow wave activity [SWS]) can be modified after learning, and in some cortical circuits, sleep is associated with replay of the learned experience. While the majority of this work has focused on neocortical and hippocampal circuits, the olfactory system may offer unique advantages as a model system for exploring sleep and memory, given the short, non-thalamic pathway from nose to primary olfactory (piriform cortex), and rapid cortex-dependent odor learning. Methodology/Principal Findings: We examined piriform cortical odor responses using local field potentials (LFPs) from freely behaving Long-Evans hooded rats over the sleep-wake cycle, and the neuronal modifications that occurred within the piriform cortex both during and after odor-fear conditioning. We also recorded LFPs from na{\"i}ve animals to characterize sleep activity in the piriform cortex and to analyze transient odor-evoked cortical responses during different sleep stages. Na{\"i}ve rats in their home cages spent 40{\%} of their time in SWS, during which the piriform cortex was significantly hypo-responsive to odor stimulation compared to awake and REM sleep states. Rats trained in the paired odor-shock conditioning paradigm developed enhanced conditioned odor evoked gamma frequency activity in the piriform cortex over the course of training compared to pseudo-conditioned rats. Furthermore, conditioned rats spent significantly more time in SWS immediately post-training both compared to pre-training days and compared to pseudo-conditioned rats. The increase in SWS immediately after training significantly correlated with the duration of odor-evoked freezing the following day. Conclusions/Significance: The rat piriform cortex is hypo-responsive to odors during SWS which accounts for nearly 40{\%} of each 24 hour period. The duration of slow-wave activity in the piriform cortex is enhanced immediately post-conditioning, and this increase is significantly correlated with subsequent memory performance. Together, these results suggest the piriform cortex may go offline during SWS to facilitate consolidation of learned odors with reduced external interference.",
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