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Changes in heart rate variability are associated with expression of short-term and long-term contextual and cued fear memories.

Liu J, Wei W, Kuang H, Zhao F, Tsien JZ - PLoS ONE (2013)

Bottom Line: We found that while fear conditioning could increase heart rate, the most significant change was the reduction in heart rate variability which could be further divided into two distinct stages: a highly rhythmic phase (stage-I) and a more variable phase (stage-II).We showed that the time duration of the stage-I rhythmic phase were sensitive enough to reflect the transition from short-term to long-term fear memories.Moreover, it could also detect fear extinction effect during the repeated tone recall.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Brain Functional Genomics, East China Normal University, Shanghai, China.

ABSTRACT
Heart physiology is a highly useful indicator for measuring not only physical states, but also emotional changes in animals. Yet changes of heart rate variability during fear conditioning have not been systematically studied in mice. Here, we investigated changes in heart rate and heart rate variability in both short-term and long-term contextual and cued fear conditioning. We found that while fear conditioning could increase heart rate, the most significant change was the reduction in heart rate variability which could be further divided into two distinct stages: a highly rhythmic phase (stage-I) and a more variable phase (stage-II). We showed that the time duration of the stage-I rhythmic phase were sensitive enough to reflect the transition from short-term to long-term fear memories. Moreover, it could also detect fear extinction effect during the repeated tone recall. These results suggest that heart rate variability is a valuable physiological indicator for sensitively measuring the consolidation and expression of fear memories in mice.

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Changes in heart rate and heart rate variability in relationships with freezing behavior during contextual recall.(A–B) The HR and CV of stage-I and stage-II freezing period in 1-hr contextual retention test. n = 11; *P<0.05, ***P<0.001, paired t test. (C) The freezing responses during contextual habituation, contextual 1-hr retention and contextual 1-day retention. n = 8; ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (D) The duration of stage-I during contextual habituation, 1-hr contextual retention and 1-day contextual retention. n = 8; ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (E–F) The CV of stage-I and stage-II during contextual habituation, 1-hr contextual retention and 1-day contextual retention. n = 8; *P<0.05, **P<0.01, one-way repeated measures ANOVA and Tukey post hoc test. (G) The averaged freezing responses in eleven mice were anti-correlated with the averaged CV of instant HR in 1-hr contextual retention (r = –0.851, P<0.001). (H) The averaged freezing responses in eight mice were also anti-correlated with the averaged CV of instant HR in 1-day contextual retention (r = –0.870, P<0.001). All data are plotted as mean ± s.e.m. (error bars).
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pone-0063590-g005: Changes in heart rate and heart rate variability in relationships with freezing behavior during contextual recall.(A–B) The HR and CV of stage-I and stage-II freezing period in 1-hr contextual retention test. n = 11; *P<0.05, ***P<0.001, paired t test. (C) The freezing responses during contextual habituation, contextual 1-hr retention and contextual 1-day retention. n = 8; ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (D) The duration of stage-I during contextual habituation, 1-hr contextual retention and 1-day contextual retention. n = 8; ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (E–F) The CV of stage-I and stage-II during contextual habituation, 1-hr contextual retention and 1-day contextual retention. n = 8; *P<0.05, **P<0.01, one-way repeated measures ANOVA and Tukey post hoc test. (G) The averaged freezing responses in eleven mice were anti-correlated with the averaged CV of instant HR in 1-hr contextual retention (r = –0.851, P<0.001). (H) The averaged freezing responses in eight mice were also anti-correlated with the averaged CV of instant HR in 1-day contextual retention (r = –0.870, P<0.001). All data are plotted as mean ± s.e.m. (error bars).

Mentions: To examine relationship between heart physiology and freezing behavior, we investigated the HR and the CV of instant HR during freezing moments. During the freezing period, the HR in stage-I was slightly but significantly higher than in stage-II (Figure 5A, P<0.05). In the meantime, HRV in stage-I was much lower than in stage-II (Figure 5B, P<0.001). Behaviorally, there were significant differences in freezing responses between contextual habituation, 1-hr contextual retention, and 1-day contextual retention tests (Figure 5C, P<0.001). We found that the durations of stage-I represented a highly correlated physiological indicator for fear memory formation (Figure 5D, P<0.001). Moreover, the CV of stage-I became tighter as the mice transit from habituation to 1-hr retention test and to 1-day retention test (Figure 5E, P<0.05). Similarly, the CV of stage-II showed the same trend (Figure 5F, P<0.01). The CV of 3-min baseline prior to 1-hr or 1-day recall showed no statistical significance from that of prior to habituation (P>0.05). The fear conditioning did not seem to have effect on basal HR dynamics.


Changes in heart rate variability are associated with expression of short-term and long-term contextual and cued fear memories.

Liu J, Wei W, Kuang H, Zhao F, Tsien JZ - PLoS ONE (2013)

Changes in heart rate and heart rate variability in relationships with freezing behavior during contextual recall.(A–B) The HR and CV of stage-I and stage-II freezing period in 1-hr contextual retention test. n = 11; *P<0.05, ***P<0.001, paired t test. (C) The freezing responses during contextual habituation, contextual 1-hr retention and contextual 1-day retention. n = 8; ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (D) The duration of stage-I during contextual habituation, 1-hr contextual retention and 1-day contextual retention. n = 8; ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (E–F) The CV of stage-I and stage-II during contextual habituation, 1-hr contextual retention and 1-day contextual retention. n = 8; *P<0.05, **P<0.01, one-way repeated measures ANOVA and Tukey post hoc test. (G) The averaged freezing responses in eleven mice were anti-correlated with the averaged CV of instant HR in 1-hr contextual retention (r = –0.851, P<0.001). (H) The averaged freezing responses in eight mice were also anti-correlated with the averaged CV of instant HR in 1-day contextual retention (r = –0.870, P<0.001). All data are plotted as mean ± s.e.m. (error bars).
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pone-0063590-g005: Changes in heart rate and heart rate variability in relationships with freezing behavior during contextual recall.(A–B) The HR and CV of stage-I and stage-II freezing period in 1-hr contextual retention test. n = 11; *P<0.05, ***P<0.001, paired t test. (C) The freezing responses during contextual habituation, contextual 1-hr retention and contextual 1-day retention. n = 8; ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (D) The duration of stage-I during contextual habituation, 1-hr contextual retention and 1-day contextual retention. n = 8; ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (E–F) The CV of stage-I and stage-II during contextual habituation, 1-hr contextual retention and 1-day contextual retention. n = 8; *P<0.05, **P<0.01, one-way repeated measures ANOVA and Tukey post hoc test. (G) The averaged freezing responses in eleven mice were anti-correlated with the averaged CV of instant HR in 1-hr contextual retention (r = –0.851, P<0.001). (H) The averaged freezing responses in eight mice were also anti-correlated with the averaged CV of instant HR in 1-day contextual retention (r = –0.870, P<0.001). All data are plotted as mean ± s.e.m. (error bars).
Mentions: To examine relationship between heart physiology and freezing behavior, we investigated the HR and the CV of instant HR during freezing moments. During the freezing period, the HR in stage-I was slightly but significantly higher than in stage-II (Figure 5A, P<0.05). In the meantime, HRV in stage-I was much lower than in stage-II (Figure 5B, P<0.001). Behaviorally, there were significant differences in freezing responses between contextual habituation, 1-hr contextual retention, and 1-day contextual retention tests (Figure 5C, P<0.001). We found that the durations of stage-I represented a highly correlated physiological indicator for fear memory formation (Figure 5D, P<0.001). Moreover, the CV of stage-I became tighter as the mice transit from habituation to 1-hr retention test and to 1-day retention test (Figure 5E, P<0.05). Similarly, the CV of stage-II showed the same trend (Figure 5F, P<0.01). The CV of 3-min baseline prior to 1-hr or 1-day recall showed no statistical significance from that of prior to habituation (P>0.05). The fear conditioning did not seem to have effect on basal HR dynamics.

Bottom Line: We found that while fear conditioning could increase heart rate, the most significant change was the reduction in heart rate variability which could be further divided into two distinct stages: a highly rhythmic phase (stage-I) and a more variable phase (stage-II).We showed that the time duration of the stage-I rhythmic phase were sensitive enough to reflect the transition from short-term to long-term fear memories.Moreover, it could also detect fear extinction effect during the repeated tone recall.

View Article: PubMed Central - PubMed

Affiliation: Key Laboratory of Brain Functional Genomics (Ministry of Education), Institute of Brain Functional Genomics, East China Normal University, Shanghai, China.

ABSTRACT
Heart physiology is a highly useful indicator for measuring not only physical states, but also emotional changes in animals. Yet changes of heart rate variability during fear conditioning have not been systematically studied in mice. Here, we investigated changes in heart rate and heart rate variability in both short-term and long-term contextual and cued fear conditioning. We found that while fear conditioning could increase heart rate, the most significant change was the reduction in heart rate variability which could be further divided into two distinct stages: a highly rhythmic phase (stage-I) and a more variable phase (stage-II). We showed that the time duration of the stage-I rhythmic phase were sensitive enough to reflect the transition from short-term to long-term fear memories. Moreover, it could also detect fear extinction effect during the repeated tone recall. These results suggest that heart rate variability is a valuable physiological indicator for sensitively measuring the consolidation and expression of fear memories in mice.

Show MeSH