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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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Comparison of heart rates and heart rate variabilities between short-term and long-term cued fear memories.(A) There was no difference in the total amount of freezing during either 30-sec tone periods or 90-sec post-tone periods between 1-hr and 1-day retention test. (B) The post-tone HR of 1-day auditory cued retention test was significantly higher than that of 1-hr retention test. n = 8; **P<0.01, paired t test. (C) The CV of during-tone and post-tone periods in 1-day auditory cued retention test was greatly reduced compared with 1-hr retention test. n = 8; *P<0.05, **P<0.01, paired t test. (D) The plateau durations during 1-day auditory cued retention were significantly longer than that during 1-hr retention. n = 8; *P<0.05, **P<0.01, paired t test. All data are plotted as mean ± s.e.m. (error bars).
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pone-0063590-g008: Comparison of heart rates and heart rate variabilities between short-term and long-term cued fear memories.(A) There was no difference in the total amount of freezing during either 30-sec tone periods or 90-sec post-tone periods between 1-hr and 1-day retention test. (B) The post-tone HR of 1-day auditory cued retention test was significantly higher than that of 1-hr retention test. n = 8; **P<0.01, paired t test. (C) The CV of during-tone and post-tone periods in 1-day auditory cued retention test was greatly reduced compared with 1-hr retention test. n = 8; *P<0.05, **P<0.01, paired t test. (D) The plateau durations during 1-day auditory cued retention were significantly longer than that during 1-hr retention. n = 8; *P<0.05, **P<0.01, paired t test. All data are plotted as mean ± s.e.m. (error bars).

Mentions: Finally, we asked how HR and HRV changes correlated with the transition and consolidation of fear memory from short-term to long-term memory. We found that there was no difference in the total amount of freezing during 30-sec tone periods between 1-hr and 1-day cued recall (Figure 8A). There was also no difference in the amount of freezing during the post-tone period between 1-hr and 1-day retention tests. This suggests that freezing scoring method is not ideal for measuring fear memories in the home cage environment. On the other hand, while the during-tone HR showed no significant difference between 1-hr and 1-day retention tests, the post-tone HR of 1-day retention was significantly higher than 1-hr retention (Figure 8B, P<0.01). Furthermore, compared with 1-hr retention test, both the CV of during-tone and post-tone periods were greatly reduced (Figure 8C, P<0.05, P<0.01). Most importantly, the durations of HRV stage-I plateau at 1-day retention tests were significantly longer than those of 1-hr retention tests (Figure 8D, P<0.05, P<0.01). The reduced CV and longer plateau duration at the time of 1-day cued memory recall show that the HRV is a valuable parameter for reflecting a more stable consolidated fear memory.


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)

Comparison of heart rates and heart rate variabilities between short-term and long-term cued fear memories.(A) There was no difference in the total amount of freezing during either 30-sec tone periods or 90-sec post-tone periods between 1-hr and 1-day retention test. (B) The post-tone HR of 1-day auditory cued retention test was significantly higher than that of 1-hr retention test. n = 8; **P<0.01, paired t test. (C) The CV of during-tone and post-tone periods in 1-day auditory cued retention test was greatly reduced compared with 1-hr retention test. n = 8; *P<0.05, **P<0.01, paired t test. (D) The plateau durations during 1-day auditory cued retention were significantly longer than that during 1-hr retention. n = 8; *P<0.05, **P<0.01, paired t test. All data are plotted as mean ± s.e.m. (error bars).
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pone-0063590-g008: Comparison of heart rates and heart rate variabilities between short-term and long-term cued fear memories.(A) There was no difference in the total amount of freezing during either 30-sec tone periods or 90-sec post-tone periods between 1-hr and 1-day retention test. (B) The post-tone HR of 1-day auditory cued retention test was significantly higher than that of 1-hr retention test. n = 8; **P<0.01, paired t test. (C) The CV of during-tone and post-tone periods in 1-day auditory cued retention test was greatly reduced compared with 1-hr retention test. n = 8; *P<0.05, **P<0.01, paired t test. (D) The plateau durations during 1-day auditory cued retention were significantly longer than that during 1-hr retention. n = 8; *P<0.05, **P<0.01, paired t test. All data are plotted as mean ± s.e.m. (error bars).
Mentions: Finally, we asked how HR and HRV changes correlated with the transition and consolidation of fear memory from short-term to long-term memory. We found that there was no difference in the total amount of freezing during 30-sec tone periods between 1-hr and 1-day cued recall (Figure 8A). There was also no difference in the amount of freezing during the post-tone period between 1-hr and 1-day retention tests. This suggests that freezing scoring method is not ideal for measuring fear memories in the home cage environment. On the other hand, while the during-tone HR showed no significant difference between 1-hr and 1-day retention tests, the post-tone HR of 1-day retention was significantly higher than 1-hr retention (Figure 8B, P<0.01). Furthermore, compared with 1-hr retention test, both the CV of during-tone and post-tone periods were greatly reduced (Figure 8C, P<0.05, P<0.01). Most importantly, the durations of HRV stage-I plateau at 1-day retention tests were significantly longer than those of 1-hr retention tests (Figure 8D, P<0.05, P<0.01). The reduced CV and longer plateau duration at the time of 1-day cued memory recall show that the HRV is a valuable parameter for reflecting a more stable consolidated fear memory.

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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