Coherent amygdalocortical theta promotes fear memory consolidation during paradoxical sleep

Institut de Biologie de l'Ecole Normale Supérieure, Centre National de la Recherche Scientifique UMR8197, Institut National de la Santé et de la Recherche Médicale U1024, 75005 Paris, France.
Proceedings of the National Academy of Sciences (Impact Factor: 9.67). 03/2010; 107(14):6516-9. DOI: 10.1073/pnas.0913016107
Source: PubMed


Brain activity in sleep plays a crucial role in memory consolidation, an offline process that determines the long-term strength of memory traces. Consolidation efficacy differs across individuals, but the brain activity dynamics underlying these differences remain unknown. Here, we studied how interindividual variability in fear memory consolidation relates to neural activity in brain structures that participate in Pavlovian fear learning. From the end of training to testing 24 h later, some rats showed increased and others decreased conditioned fear responses. We found that overnight bidirectional changes in fear memory were selectively correlated with modifications in theta coherence between the amygdala, medial prefrontal cortex, and hippocampus during paradoxical sleep. Thus, our results suggest that theta coordination in the limbic system may influence interindividual differences in memory consolidation of aversive experiences.

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    • "Synchronous oscillatory activity between HPC and BLA represents an intermediate phenomenon to link the firing of single neurons to behavior (Paré et al., 2002). Theta synchronization of lateral amygdala (LA) and CA1 HPC increases during fear memory retrieval in rodents (Seidenbecher et al., 2003), and the degree of theta synchrony predicts memory performance after fear conditioning (Popa et al., 2010). Likewise, dynamic shifts in theta synchrony of CA1, BLA, and medial prefrontal cortex (mPFC) are associated with ongoing defensive behavior (Likhtik et al., 2014) and extinction of conditioned fear (Lesting et al., 2011). "
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    ABSTRACT: The dynamic interactions between hippocampus and amygdala are critical for emotional memory. Theta synchrony between these structures occurs during fear memory retrieval and may facilitate synaptic plasticity, but the cellular mechanisms are unknown. We report that interneurons of the mouse basal amygdala are activated during theta network activity or optogenetic stimulation of ventral CA1 pyramidal cell axons, whereas principal neurons are inhibited. Interneurons provide feedforward inhibition that transiently hyperpolarizes principal neurons. However, synaptic inhibition attenuates during theta frequency stimulation of ventral CA1 fibers, and this broadens excitatory postsynaptic potentials. These effects are mediated by GABAB receptors and change in the Cl− driving force. Pairing theta frequency stimulation of ventral CA1 fibers with coincident stimuli of the lateral amygdala induces long-term potentiation of lateral-basal amygdala excitatory synapses. Hence, feedforward inhibition, known to enforce temporal fidelity of excitatory inputs, dominates hippocampus-amygdala interactions to gate heterosynaptic plasticity. Video Abstract
    Full-text · Article · Sep 2015 · Neuron
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    • "Critically, overnight changes in fear memory were correlated specifically with theta coherence in limbic and medial prefrontal regions during rapid eye movement (REM) sleep (Popa et al. 2010). Moreover, it has been shown that pretraining REM SD has detrimental effects on avoidance learning in rats (Gruart-Masso et al. 1995), further suggesting that REM sleep could be of particular interest in this context. "
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    ABSTRACT: Sleep disturbances are prevalent in clinical anxiety but it remains unclear whether they are cause and/or consequence of this condition. Fear conditioning constitutes a valid laboratory model for the acquisition of normal and pathological anxiety. To explore the relationship between disturbed sleep and anxiety in more detail, the present study evaluated the effect of partial sleep deprivation (SD) on fear conditioning in healthy individuals. The neural correlates of (1) non-associative learning and physiological processing, and (2) associative learning (differential fear conditioning) were addressed. Measurements entailed simultaneous functional magnetic resonance imaging (fMRI), electroencephalography (EEG), skin conductance response (SCR) and pulse recordings. Regarding non-associative learning (1), partial SD resulted in a generalized failure to habituate during fear conditioning as evidenced by reduced habituation of SCR and hypothalamus responses to all stimuli. Furthermore, SCR and hypothalamus activity were correlated, supporting their functional relationship. Regarding associative learning (2) effects of partial SD on the acquisition of conditioned fear were weaker and did not reach statistical significance. The hypothalamus plays an integral role in the regulation of sleep and autonomic arousal. Thus, sleep disturbances may play a causal role in the development of normal and, possibly, pathological fear by increasing the susceptibility of the sympathetic nervous system to stressful experiences.
    Full-text · Article · Jun 2014 · Journal of Neurophysiology
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    • "As is true for increases in neuronal firing, it seems plausible that enhancing theta-oscillations could promote consolidation by creating optimal conditions for synaptic potentiation within hippocampal circuits. Moreover, because increased theta-frequency coherence between the hippocampus and other brain areas (e.g., the amygdala and prefrontal cortex) is specifically associated with other forms of memory consolidation (Benchenane et al., 2010; Popa et al., 2010), it is also possible that enhanced CA1 theta-rhythms could drive systems-level memory consolidation during sleep (Aton et al., 2009b). "
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    ABSTRACT: A period of sleep over the first few hours following single-trial contextual fear conditioning (CFC) is essential for hippocampally-mediated memory consolidation. Recent studies have uncovered intracellular mechanisms required for memory formation which are affected by post-conditioning sleep and sleep deprivation. However, almost nothing is known about the circuit-level activity changes during sleep that underlie activation of these intracellular pathways. Here we continuously recorded from the CA1 region of freely-behaving mice to characterize neuronal and network activity changes occurring during active memory consolidation. C57BL/6J mice were implanted with custom stereotrode recording arrays to monitor activity of individual CA1 neurons, local field potentials (LFPs), and electromyographic activity. Sleep architecture and state-specific CA1 activity patterns were assessed during a 24 h baseline recording period, and for 24 h following either single-trial CFC or Sham conditioning. We find that consolidation of CFC is not associated with significant sleep architecture changes, but is accompanied by long-lasting increases in CA1 neuronal firing, as well as increases in delta, theta, and gamma-frequency CA1 LFP activity. These changes occurred in both sleep and wakefulness, and may drive synaptic plasticity within the hippocampus during memory formation. We also find that functional connectivity within the CA1 network, assessed through functional clustering algorithm (FCA) analysis of spike timing relationships among recorded neurons, becomes more stable during consolidation of CFC. This increase in network stability was not present following Sham conditioning, was most evident during post-CFC slow wave sleep (SWS), and was negligible during post-CFC wakefulness. Thus in the interval between encoding and recall, SWS may stabilize the hippocampal contextual fear memory (CFM) trace by promoting CA1 network stability.
    Full-text · Article · Apr 2014 · Frontiers in Systems Neuroscience
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