Fear Extinction Memory Consolidation Requires Potentiation of Pontine-Wave Activity during REM Sleep
ABSTRACT Sleep plays an important role in memory consolidation within multiple memory systems including contextual fear extinction memory, but little is known about the mechanisms that underlie this process. Here, we show that fear extinction training in rats, which extinguished conditioned fear, increased both slow-wave sleep and rapid-eye movement (REM) sleep. Surprisingly, 24 h later, during memory testing, only 57% of the fear-extinguished animals retained fear extinction memory. We found that these animals exhibited an increase in phasic pontine-wave (P-wave) activity during post-training REM sleep, which was absent in the 43% of animals that failed to retain fear extinction memory. The results of this study provide evidence that brainstem activation, specifically potentiation of phasic P-wave activity, during post-training REM sleep is critical for consolidation of fear extinction memory. The results of this study also suggest that, contrary to the popular hypothesis of sleep and memory, increased sleep after training alone does not guarantee consolidation and/or retention of fear extinction memory. Rather, the potentiation of specific sleep-dependent physiological events may be a more accurate predictor for successful consolidation of fear extinction memory. Identification of this unique mechanism will significantly improve our present understanding of the cellular and molecular mechanisms that underlie the sleep-dependent regulation of emotional memory. Additionally, this discovery may also initiate development of a new, more targeted treatment method for clinical disorders of fear and anxiety in humans that is more efficacious than existing methods such as exposure therapy that incorporate only fear extinction.
- SourceAvailable from: Donald A Wilson
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- "REM sleep is characterized by fast, low-amplitude oscillatory activity in the θ-band (4–8 Hz) and higher frequency bands characteristic of waking (van der Helm et al., 2011). REM sleep also includes ponto-geniculo-occipital (PGO) waves that are intense bursts of synchronized activity propagating from the pontine region of the brain stem to the lateral geniculate nucleus and visual cortex (Datta and O’Malley, 2013). Behavioral hallmarks of REM sleep are phasic bouts of REM (hence the phase’s name) and muscle atonia (Jones, 1979). "
ABSTRACT: In many systems, sleep plays a vital role in memory consolidation and synaptic homeostasis. These processes together help store information of biological significance and reset synaptic circuits to facilitate acquisition of information in the future. In this review, we describe recent evidence of sleep-dependent changes in olfactory system structure and function which contribute to odor memory and perception. During slow-wave sleep, the piriform cortex becomes hypo-responsive to odor stimulation and instead displays sharp-wave activity similar to that observed within the hippocampal formation. Furthermore, the functional connectivity between the piriform cortex and other cortical and limbic regions is enhanced during slow-wave sleep compared to waking. This combination of conditions may allow odor memory consolidation to occur during a state of reduced external interference and facilitate association of odor memories with stored hedonic and contextual cues. Evidence consistent with sleep-dependent odor replay within olfactory cortical circuits is presented. These data suggest that both the strength and precision of odor memories is sleep-dependent. The work further emphasizes the critical role of synaptic plasticity and memory in not only odor memory but also basic odor perception. The work also suggests a possible link between sleep disturbances that are frequently co-morbid with a wide range of pathologies including Alzheimer's disease, schizophrenia and depression and the known olfactory impairments associated with those disorders.Frontiers in Behavioral Neuroscience 04/2014; 8:134. DOI:10.3389/fnbeh.2014.00134 · 3.27 Impact Factor
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- "Effects of sleep on learned response inhibition have so far been mainly examined using fear extinction paradigms. The studies consistently showed a beneficial effect of sleep on fear extinction learning in rats and humans that was linked to both signs of NonREM sleep and REM sleep (e.g., Pace-Schott et al. 2012; Spoormaker et al. 2012; Kleim et al. 2013; Datta and O’Malley 2013; Fu et al. 2007; Silvestri 2005). Whereas the present study is limited in that it did not apply electrophysiological recordings to differentiate specific sleep stages, it adds to those previous observations in demonstrating a robust sleep benefit for learned response inhibition using an appetitive, rather than aversive, behavioral approach in which inhibitory memory might be differently mediated. "
ABSTRACT: Sleep supports the consolidation of memory, and it has been proposed that this enhancing effect of sleep pertains in particular to memories which are encoded under control of prefrontal-hippocampal circuitry into an episodic memory system. Furthermore, repeated reactivation and transformation of such memories during sleep are thought to promote the de-contextualization of these memories. Here, we aimed to establish a behavioral model for the study of such sleep-dependent system consolidation in rats, using a go/nogo conditional discrimination learning task known to essentially depend on prefrontal-hippocampal function. Different groups of rats were trained to criterion on this task and, then, subjected to 80-min retention intervals filled with spontaneous morning sleep, sleep deprivation, or spontaneous evening wakefulness. In a subsequent test phase, the speed of relearning of the discrimination task was examined as indicator of memory, whereby rats were either tested in the same context as during training or in a different context. Sleep promoted relearning of the conditional discrimination task, and this effect was similar for testing memory in the same or different context (p < 0.001). Independent of sleep and wakefulness during the retention interval, animals showed faster relearning when tested in the same context as during learning, compared with testing in a different context (p < 0.001). The benefitting effect of sleep on discrimination learning was primarily due to an enhancing effect on response suppression during the nogo stimulus. We infer from these results that sleep enhances memory for inhibitory behavioral control in a generalized context-independent manner and thereby might eventually also contribute to the abstraction of schema-like representations.Experimental Brain Research 12/2013; 232(5). DOI:10.1007/s00221-013-3797-5 · 2.04 Impact Factor
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ABSTRACT: The symptoms we identify and the behaviors we recognize as defenses define which symptoms we see as trauma-related. Early conceptions of trauma-related disorders focused on physical signs of distress while current ones emphasize mental symptoms, but traumatizing experiences evoke psychobiological reactions. An evolutionary perspective presumes that psychophysical reactions to traumatizing events evolved to ensure survival. This theoretical review examines several primitive mechanisms (e.g., sensitization and dissolution) associated with responses to diverse stressors, from danger to life-threat. Some rapidly acquired symptoms form without conscious awareness because severe stresses can dysregulate mental and physical components within systems ensuring survival. Varied defensive options engage specialized and enduring psychophysical reactions; this allows for more adaptive responses to diverse threats. Thus, parasympathetically mediated defense states such as freeze or collapse increase trauma-related symptom variability. Comorbidity and symptom variability confuse those expecting mental rather than psychophysical responses to trauma, and active (sympathetically mediated flight and fight) rather than immobility defenses. Healthcare implications for stress research, clinical practice and diagnostic nosology stem from the broader evolutionary view.Neuroscience & Biobehavioral Reviews 06/2013; 37(8). DOI:10.1016/j.neubiorev.2013.06.004 · 8.80 Impact Factor