Neuronal plasticity induced by fear conditioning is expressed during paradoxical sleep: Evidence from simultaneous recordings in the lateral amygdala and the medial geniculate in rats.

Hennevin, Elizabeth; Maho, Catherine; Hars, Bernard

doi:10.1037/0735-7044.112.4.839

Cited by 45 publications

(48 citation statements)

References 149 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…With this background, it is tempting to relate the particular benefit for emotional memory from late retention sleep to enhanced amygdalar activity accompanying the extended REM sleep epochs of this period. This conclusion is also supported by several other studies in animals and humans suggesting that patterns of emotional arousal induced during learning become reactivated during REM sleep, thereby strengthening memory traces and connectivity within respective neural networks (Goodenough et al 1975;Hennevin et al 1998;Maho and Hennevin 1999). In the case of emotional declarative memories, this influence could be mediated via modulatory influences of the amygdala on the hippocampal memory system Hamann et al 1999;Roozendaal 2000).…”

Section: Emotional Memory and Rem Sleepsupporting

confidence: 71%

Emotional Memory Formation Is Enhanced across Sleep Intervals with High Amounts of Rapid Eye Movement Sleep

Wagner¹,

Gais²,

Born³

2001

Learn. Mem.

526

387

View full text Add to dashboard Cite

Recent studies indicated a selective activation during rapid eye movement (REM) sleep of the amygdala known to play a decisive role in the processing of emotional stimuli. This study compared memory retention of emotional versus neutral text material over intervals covering either early sleep known to be dominated by nonREM slow wave sleep (SWS) or late sleep, in which REM sleep is dominant. Two groups of men were tested across 3-h periods of early and late sleep (sleep group) or corresponding retention intervals filled with wakefulness (wake group). Sleep was recorded polysomnographically. Cortisol concentrations in saliva were monitored at acquisition and retrieval testing. As expected, the amount of REM sleep was about three times greater during late than during early retention sleep, whereas a reversed pattern was observed for SWS distribution (P < 0.001). Sleep improved retention, compared with the effects of wake intervals (P < 0.02). However, this effect was substantial only in the late night (P < 0.005), during which retention was generally worse than during the early night (P < 0.02). Late sleep particularly enhanced memory for emotional texts. This effect was highly significant in comparison with memory for neutral texts (P < 0.01) and in comparison with memory after late and early wake intervals (P < 0.001). Cortisol concentration differed between early and late retention intervals but not between sleep and wake conditions. Results are consonant with a supportive function of REM sleep predominating late sleep for the formation of emotional memory in humans.It is well established that sleep has a facilitating effect on memory formation in animals and humans (e.g., Jenkins and Dallenbach 1924;Smith 1985Smith , 1995Stickgold et al. 2000). However, the physiological mechanisms of this effect are still unclear. Specifically, there is an ongoing controversy concerning the differential contribution of rapid eye movement (REM) sleep and slow wave sleep (SWS) to memory consolidation. In particular, human studies provided mixed results, some indicating a beneficial effect of REM sleep on memory (Empson and Clarke 1970;Lewin and Glaubman 1975;Tilley and Empson 1978) whereas others suggested SWS to be critical for memory formation (Yaroush et al. 1971;Barrett and Ekstrand 1972;Fowler et al. 1973;Ekstrand 1977). The divergent outcomes appear to reflect differences in the methods used for investigating memory formation during sleep and in the type of memory examined. The most commonly used approach in the study of sleepassociated memory formation is the REM sleep deprivation paradigm, in which subjects are awakened whenever polysomnographic recordings indicate signs of REM sleep. In control conditions, awakenings are induced in nonREM sleep. Yet the REM sleep-deprivation paradigm has been subject to profound criticism (Horne and McGrath 1984; Vertes and Eastman, in press). Compared with other sleep stages, frequent arousal from REM sleep induces serious emotional and cognitive disturbances. These disturbances impa...

show abstract

Section: Emotional Memory and Rem Sleepsupporting

confidence: 71%

Emotional Memory Formation Is Enhanced across Sleep Intervals with High Amounts of Rapid Eye Movement Sleep

Wagner¹,

Gais²,

Born³

2001

Learn. Mem.

526

387

View full text Add to dashboard Cite

show abstract

“…In the control period, the CS + and CS − evoked an increase in EMG activity of the posterior neck muscles whereas after pairing, the CS + , but not the CS − , elicited a reduction in EMG activity. This result might seem surprising as, following fear conditioning, freely moving rats were reported to exhibit increased CS-evoked EMG responses associated with freezing (Hennevin et al 1998). We speculate that our counterintuitive finding is a consequence of the head restraint imposed on the animals.…”

Section: Nature Of the Conditioned Emg Responsescontrasting

confidence: 49%

Differential Fear Conditioning Induces Reciprocal Changes in the Sensory Responses of Lateral Amygdala Neurons to the CS⁺ and CS⁻

Collins¹,

Paré²

2000

Learn. Mem.

159

View full text Add to dashboard Cite

In classical fear conditioning, a neutral sensory stimulus (CS) acquires the ability to elicit fear responses after pairing to a noxious unconditioned stimulus (US). As amygdala lesions prevent the acquisition of fear responses and the lateral amygdaloid (LA) nucleus is the main input station of the amygdala for auditory afferents, the effect of auditory fear conditioning on the sensory responsiveness of LA neurons has been examined. Although conditioning was shown to increase CS-evoked LA responses, the specificity of the changes in responsiveness was not tested. Because conditioning might induce nonspecific increases in LA responses to auditory afferents, we re-examined this issue in conscious, head-restrained cats using a differential conditioning paradigm where only one of two tones (CS + but not CS − ) was paired to the US. Differential conditioning increased unit and field responses to the CS + , whereas responses to the CS − decreased. Such changes have never been observed in the amygdala except in cases where the CS − had been paired to the US before and fear responses not extinguished. This suggests that fear conditioning is not only accompanied by potentiation of amygdalopetal pathways conveying the CS + but also by the depression of sensory inputs unpaired to noxious stimuli.The amygdaloid complex is a nucleated structure of the temporal lobe receiving sensory inputs of all modalities and projecting to functionally diverse brain structures, from the highest computational levels of the brain to hypothalamic and brainstem autonomic nuclei involved in cardiovascular control and the expression of species-specific fear responses (Hopkins and Holstege 1978;Price and Amaral 1981;Bandler 1982;Veening et al. 1984;Russchen 1986;Amaral et al. 1992).Much evidence implicates the amygdala in fear learning and expression. For instance, stimulation of the central amygdaloid nucleus elicits increases in heart rate and blood pressure (Kaada 1972;Iwata et al. 1987). Moreover, amygdala lesions prevent the acquisition of classically conditioned fear responses (Kapp et al. 1979;Gentile et al. 1986;Iwata et al. 1986;Hitchcock and Davis 1987;LeDoux et al. 1990b;Killcross et al. 1997). These and other findings (for review, see Davis 1992; LeDoux 1995) have prompted investigators to search for the cellular correlates of fear learning in the amygdala.As the lateral amygdaloid (LA) nucleus is the main input station of the amygdala for auditory afferents (LeDoux et al. 1990a,b;Romanski and LeDoux 1992), a few studies have examined how auditory fear conditioning affects toneevoked LA responses (Quirk et al. 1995;Rogan et al. 1997). These studies reported that fear conditioning increases auditory-evoked responses in the LA. These changes in responsiveness were not a simple consequence of the arousal produced by the unconditioned stimulus (US) as they were not observed when the auditory conditioned stimulus (CS) and the US were presented in an unpaired manner. However, the possibility that the CS-US pairings induced nonspecific inc...

show abstract

“…Conditioned responses to tone paired with shock during the awake state can be expressed in both the hippocampus and the medial geniculate nucleus during sleep (Hennevin et al 1993). Conditioned neuronal responses in the amygdala, which probably mediates the affective component of the memory, are likewise elicited by the CS during REM sleep (Hennevin et al 1998).…”

Section: Memory Reactivation and Consolidation During Sleepmentioning

confidence: 99%

Retrieval and Reconsolidation: Toward a Neurobiology of Remembering

Sara¹

2000

Learn. Mem.

838

580

View full text Add to dashboard Cite

Neuronal plasticity induced by fear conditioning is expressed during paradoxical sleep: Evidence from simultaneous recordings in the lateral amygdala and the medial geniculate in rats.

Cited by 45 publications

References 149 publications

Emotional Memory Formation Is Enhanced across Sleep Intervals with High Amounts of Rapid Eye Movement Sleep

Emotional Memory Formation Is Enhanced across Sleep Intervals with High Amounts of Rapid Eye Movement Sleep

Differential Fear Conditioning Induces Reciprocal Changes in the Sensory Responses of Lateral Amygdala Neurons to the CS⁺ and CS⁻

Retrieval and Reconsolidation: Toward a Neurobiology of Remembering

Contact Info

Product

Resources

About

Neuronal plasticity induced by fear conditioning is expressed during paradoxical sleep: Evidence from simultaneous recordings in the lateral amygdala and the medial geniculate in rats.

Cited by 45 publications

References 149 publications

Emotional Memory Formation Is Enhanced across Sleep Intervals with High Amounts of Rapid Eye Movement Sleep

Emotional Memory Formation Is Enhanced across Sleep Intervals with High Amounts of Rapid Eye Movement Sleep

Differential Fear Conditioning Induces Reciprocal Changes in the Sensory Responses of Lateral Amygdala Neurons to the CS+ and CS−

Retrieval and Reconsolidation: Toward a Neurobiology of Remembering

Contact Info

Product

Resources

About

Differential Fear Conditioning Induces Reciprocal Changes in the Sensory Responses of Lateral Amygdala Neurons to the CS⁺ and CS⁻