Limits...
Stimulus-specific enhancement of fear extinction during slow-wave sleep.

Hauner KK, Howard JD, Zelano C, Gottfried JA - Nat. Neurosci. (2013)

Bottom Line: Sleep can strengthen memory for emotional information, but whether emotional memories can be specifically targeted and modified during sleep is unknown.In human subjects who underwent olfactory contextual fear conditioning, re-exposure to the odorant context in slow-wave sleep promoted stimulus-specific fear extinction, with parallel reductions of hippocampal activity and reorganization of amygdala ensemble patterns.Thus, fear extinction may be selectively enhanced during sleep, even without re-exposure to the feared stimulus itself.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA.

ABSTRACT
Sleep can strengthen memory for emotional information, but whether emotional memories can be specifically targeted and modified during sleep is unknown. In human subjects who underwent olfactory contextual fear conditioning, re-exposure to the odorant context in slow-wave sleep promoted stimulus-specific fear extinction, with parallel reductions of hippocampal activity and reorganization of amygdala ensemble patterns. Thus, fear extinction may be selectively enhanced during sleep, even without re-exposure to the feared stimulus itself.

Show MeSH

Related in: MedlinePlus

Sleep-related modulatory effects of target odorant re-exposure on fMRI activity(a) Activity evoked by tgCS+ (vs. ntCS+) was reduced from pre- to post-sleep in anterior hippocampus (t[14]=−4.65, **P<0.001; adjusted for CS− baselines). Activation maps are overlaid on a T1-weighted coronal section from a representative subject (display threshold, P<0.005). Box plots (right) indicate median (central line) and upper/lower quartiles (top/bottom of box) for each condition. Whiskers denote extent of data between 10th and 90th percentiles. (b) Post-sleep (vs. pre-sleep) activity in entorhinal cortex evoked by tgCS+ (vs. ntCS+) was negatively correlated with the duration of odorant re-exposure during SWS (r=−0.51, P=0.05, n=15). (c) (Left) Voxel-wise ensemble maps of left amygdala activity from one subject show that condition-specific patterns diverged more for tgCS+ (vs. ntCS+) from pre- to post-sleep. Each square represents signal intensity from a different voxel (n=75), arranged in columns from top left to bottom right, in ascending order for tgCS+ in the pre-sleep condition. (Right) Across all subjects, pre- and post-sleep pattern ensembles in amygdala became more distinct (less correlated) for tgCS+ compared to ntCS+ (t[14]=−2.66, *P=0.02; adjusted for CS− baselines; paired t test).
© Copyright Policy
Related In: Results  -  Collection


getmorefigures.php?uid=PMC3818116&req=5

Figure 2: Sleep-related modulatory effects of target odorant re-exposure on fMRI activity(a) Activity evoked by tgCS+ (vs. ntCS+) was reduced from pre- to post-sleep in anterior hippocampus (t[14]=−4.65, **P<0.001; adjusted for CS− baselines). Activation maps are overlaid on a T1-weighted coronal section from a representative subject (display threshold, P<0.005). Box plots (right) indicate median (central line) and upper/lower quartiles (top/bottom of box) for each condition. Whiskers denote extent of data between 10th and 90th percentiles. (b) Post-sleep (vs. pre-sleep) activity in entorhinal cortex evoked by tgCS+ (vs. ntCS+) was negatively correlated with the duration of odorant re-exposure during SWS (r=−0.51, P=0.05, n=15). (c) (Left) Voxel-wise ensemble maps of left amygdala activity from one subject show that condition-specific patterns diverged more for tgCS+ (vs. ntCS+) from pre- to post-sleep. Each square represents signal intensity from a different voxel (n=75), arranged in columns from top left to bottom right, in ascending order for tgCS+ in the pre-sleep condition. (Right) Across all subjects, pre- and post-sleep pattern ensembles in amygdala became more distinct (less correlated) for tgCS+ compared to ntCS+ (t[14]=−2.66, *P=0.02; adjusted for CS− baselines; paired t test).

Mentions: Next, we used fMRI to examine how sleep-mediated fear extinction is implemented in the human brain. A key region of interest was the hippocampal formation, involved in contextual fear conditioning11,12 and retrieval13, and in SWS-mediated memory consolidation2,5. Whole-brain analyses revealed a decline in stimulus-evoked mean fMRI activity for tgCS+ (vs. ntCS+) from pre- to post-sleep in right anterior hippocampus (P=0.0003, cross-validated; small-volume corrected; Fig. 2a), anterior cingulate cortex (ACC), and insula (Supplementary Table 2). Furthermore, odorant re-exposure duration (during SWS) was negatively correlated with tgCS+-evoked activity in right entorhinal cortex (r=−0.51, P=0.05, cross-validated; Fig. 2b), a region providing substantial afferent input to hippocampus14. These reductions in fMRI activity accord with the roles of these regions in contextual retrieval (hippocampus, entorhinal cortex)13 and expression (ACC, insula)10 of fear memory.


Stimulus-specific enhancement of fear extinction during slow-wave sleep.

Hauner KK, Howard JD, Zelano C, Gottfried JA - Nat. Neurosci. (2013)

Sleep-related modulatory effects of target odorant re-exposure on fMRI activity(a) Activity evoked by tgCS+ (vs. ntCS+) was reduced from pre- to post-sleep in anterior hippocampus (t[14]=−4.65, **P<0.001; adjusted for CS− baselines). Activation maps are overlaid on a T1-weighted coronal section from a representative subject (display threshold, P<0.005). Box plots (right) indicate median (central line) and upper/lower quartiles (top/bottom of box) for each condition. Whiskers denote extent of data between 10th and 90th percentiles. (b) Post-sleep (vs. pre-sleep) activity in entorhinal cortex evoked by tgCS+ (vs. ntCS+) was negatively correlated with the duration of odorant re-exposure during SWS (r=−0.51, P=0.05, n=15). (c) (Left) Voxel-wise ensemble maps of left amygdala activity from one subject show that condition-specific patterns diverged more for tgCS+ (vs. ntCS+) from pre- to post-sleep. Each square represents signal intensity from a different voxel (n=75), arranged in columns from top left to bottom right, in ascending order for tgCS+ in the pre-sleep condition. (Right) Across all subjects, pre- and post-sleep pattern ensembles in amygdala became more distinct (less correlated) for tgCS+ compared to ntCS+ (t[14]=−2.66, *P=0.02; adjusted for CS− baselines; paired t test).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3818116&req=5

Figure 2: Sleep-related modulatory effects of target odorant re-exposure on fMRI activity(a) Activity evoked by tgCS+ (vs. ntCS+) was reduced from pre- to post-sleep in anterior hippocampus (t[14]=−4.65, **P<0.001; adjusted for CS− baselines). Activation maps are overlaid on a T1-weighted coronal section from a representative subject (display threshold, P<0.005). Box plots (right) indicate median (central line) and upper/lower quartiles (top/bottom of box) for each condition. Whiskers denote extent of data between 10th and 90th percentiles. (b) Post-sleep (vs. pre-sleep) activity in entorhinal cortex evoked by tgCS+ (vs. ntCS+) was negatively correlated with the duration of odorant re-exposure during SWS (r=−0.51, P=0.05, n=15). (c) (Left) Voxel-wise ensemble maps of left amygdala activity from one subject show that condition-specific patterns diverged more for tgCS+ (vs. ntCS+) from pre- to post-sleep. Each square represents signal intensity from a different voxel (n=75), arranged in columns from top left to bottom right, in ascending order for tgCS+ in the pre-sleep condition. (Right) Across all subjects, pre- and post-sleep pattern ensembles in amygdala became more distinct (less correlated) for tgCS+ compared to ntCS+ (t[14]=−2.66, *P=0.02; adjusted for CS− baselines; paired t test).
Mentions: Next, we used fMRI to examine how sleep-mediated fear extinction is implemented in the human brain. A key region of interest was the hippocampal formation, involved in contextual fear conditioning11,12 and retrieval13, and in SWS-mediated memory consolidation2,5. Whole-brain analyses revealed a decline in stimulus-evoked mean fMRI activity for tgCS+ (vs. ntCS+) from pre- to post-sleep in right anterior hippocampus (P=0.0003, cross-validated; small-volume corrected; Fig. 2a), anterior cingulate cortex (ACC), and insula (Supplementary Table 2). Furthermore, odorant re-exposure duration (during SWS) was negatively correlated with tgCS+-evoked activity in right entorhinal cortex (r=−0.51, P=0.05, cross-validated; Fig. 2b), a region providing substantial afferent input to hippocampus14. These reductions in fMRI activity accord with the roles of these regions in contextual retrieval (hippocampus, entorhinal cortex)13 and expression (ACC, insula)10 of fear memory.

Bottom Line: Sleep can strengthen memory for emotional information, but whether emotional memories can be specifically targeted and modified during sleep is unknown.In human subjects who underwent olfactory contextual fear conditioning, re-exposure to the odorant context in slow-wave sleep promoted stimulus-specific fear extinction, with parallel reductions of hippocampal activity and reorganization of amygdala ensemble patterns.Thus, fear extinction may be selectively enhanced during sleep, even without re-exposure to the feared stimulus itself.

View Article: PubMed Central - PubMed

Affiliation: Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, Illinois, USA.

ABSTRACT
Sleep can strengthen memory for emotional information, but whether emotional memories can be specifically targeted and modified during sleep is unknown. In human subjects who underwent olfactory contextual fear conditioning, re-exposure to the odorant context in slow-wave sleep promoted stimulus-specific fear extinction, with parallel reductions of hippocampal activity and reorganization of amygdala ensemble patterns. Thus, fear extinction may be selectively enhanced during sleep, even without re-exposure to the feared stimulus itself.

Show MeSH
Related in: MedlinePlus