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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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ECG recording during four behavioral states.(A) Illustration of the proper ECG electrodes implantation sites on a mouse. The negative electrode (-) was implanted in the mouse’s right upper chest, and the positive electrode (+) was placed in the left abdomen. (B) Three consecutive cycles of heart beats as example of ECG recording. The peaks are labeled by conventional ECG terminology. Inset: average waveform of individual heart beats recorded in 1 minute, centered on the peak of the R-wave. (C) Mean heart rate of mice during four basic behavioral states in the home cage. AW, active wakefulness; QW, quiet wakefulness; REM, rapid eye movement sleep; SWS, slow wave sleep. Error bars, s.e.m.; n = 5; **P<0.01, ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (D) Examples of 30-sec instant HR and 2-sec ECG and hippocampal CA1 LFPs during AW, QW, REM and SWS from an individual mouse. The red dots indicate the peaks of the R-wave. Scales: 0.5 mV. (E) Poincaré plot analysis graphed the same mouse’s R-R interval data of four 1-min periods: during AW, QW, REM and SWS. Successive points in the plots were connected with a line.
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pone-0063590-g001: ECG recording during four behavioral states.(A) Illustration of the proper ECG electrodes implantation sites on a mouse. The negative electrode (-) was implanted in the mouse’s right upper chest, and the positive electrode (+) was placed in the left abdomen. (B) Three consecutive cycles of heart beats as example of ECG recording. The peaks are labeled by conventional ECG terminology. Inset: average waveform of individual heart beats recorded in 1 minute, centered on the peak of the R-wave. (C) Mean heart rate of mice during four basic behavioral states in the home cage. AW, active wakefulness; QW, quiet wakefulness; REM, rapid eye movement sleep; SWS, slow wave sleep. Error bars, s.e.m.; n = 5; **P<0.01, ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (D) Examples of 30-sec instant HR and 2-sec ECG and hippocampal CA1 LFPs during AW, QW, REM and SWS from an individual mouse. The red dots indicate the peaks of the R-wave. Scales: 0.5 mV. (E) Poincaré plot analysis graphed the same mouse’s R-R interval data of four 1-min periods: during AW, QW, REM and SWS. Successive points in the plots were connected with a line.

Mentions: We implanted a single pair of electrodes into mouse’s right upper chest and left abdomen to allow recording of electrocardiogram (ECG) signals (Figure 1A). Data from 11 mice were included in the current analyses. The typical peaks in heart beats could be clearly identified with the timestamps of R-wave peaks (Figure 1B). To provide the overall characterization of HR dynamics in mice, we employed hippocampal local field potentials (LFPs) to classify mouse behavior into four basic states in the home cage: namely, active wakefulness (AW), quiet wakefulness (QW), rapid eye movement (REM) sleep and slow wave sleep (SWS). We calculated the mean HR during these states and found averaged HR as follows: 597±12 bpm for AW, 507±18 bpm for QW, 493±20 bpm for REM, and 449±26 bpm for SWS (Figure 1C). The HR during AW was significantly higher than during QW, REM and SWS states (Figure 1C, P<0.01, P<0.001). The HR during QW, REM and SWS showed no significant difference between each other (Figure 1C, QW:REM, P = 0.956; QW:SWS, P = 0.098; REM:SWS, P = 0.215).


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)

ECG recording during four behavioral states.(A) Illustration of the proper ECG electrodes implantation sites on a mouse. The negative electrode (-) was implanted in the mouse’s right upper chest, and the positive electrode (+) was placed in the left abdomen. (B) Three consecutive cycles of heart beats as example of ECG recording. The peaks are labeled by conventional ECG terminology. Inset: average waveform of individual heart beats recorded in 1 minute, centered on the peak of the R-wave. (C) Mean heart rate of mice during four basic behavioral states in the home cage. AW, active wakefulness; QW, quiet wakefulness; REM, rapid eye movement sleep; SWS, slow wave sleep. Error bars, s.e.m.; n = 5; **P<0.01, ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (D) Examples of 30-sec instant HR and 2-sec ECG and hippocampal CA1 LFPs during AW, QW, REM and SWS from an individual mouse. The red dots indicate the peaks of the R-wave. Scales: 0.5 mV. (E) Poincaré plot analysis graphed the same mouse’s R-R interval data of four 1-min periods: during AW, QW, REM and SWS. Successive points in the plots were connected with a line.
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Related In: Results  -  Collection

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pone-0063590-g001: ECG recording during four behavioral states.(A) Illustration of the proper ECG electrodes implantation sites on a mouse. The negative electrode (-) was implanted in the mouse’s right upper chest, and the positive electrode (+) was placed in the left abdomen. (B) Three consecutive cycles of heart beats as example of ECG recording. The peaks are labeled by conventional ECG terminology. Inset: average waveform of individual heart beats recorded in 1 minute, centered on the peak of the R-wave. (C) Mean heart rate of mice during four basic behavioral states in the home cage. AW, active wakefulness; QW, quiet wakefulness; REM, rapid eye movement sleep; SWS, slow wave sleep. Error bars, s.e.m.; n = 5; **P<0.01, ***P<0.001, one-way repeated measures ANOVA and Tukey post hoc test. (D) Examples of 30-sec instant HR and 2-sec ECG and hippocampal CA1 LFPs during AW, QW, REM and SWS from an individual mouse. The red dots indicate the peaks of the R-wave. Scales: 0.5 mV. (E) Poincaré plot analysis graphed the same mouse’s R-R interval data of four 1-min periods: during AW, QW, REM and SWS. Successive points in the plots were connected with a line.
Mentions: We implanted a single pair of electrodes into mouse’s right upper chest and left abdomen to allow recording of electrocardiogram (ECG) signals (Figure 1A). Data from 11 mice were included in the current analyses. The typical peaks in heart beats could be clearly identified with the timestamps of R-wave peaks (Figure 1B). To provide the overall characterization of HR dynamics in mice, we employed hippocampal local field potentials (LFPs) to classify mouse behavior into four basic states in the home cage: namely, active wakefulness (AW), quiet wakefulness (QW), rapid eye movement (REM) sleep and slow wave sleep (SWS). We calculated the mean HR during these states and found averaged HR as follows: 597±12 bpm for AW, 507±18 bpm for QW, 493±20 bpm for REM, and 449±26 bpm for SWS (Figure 1C). The HR during AW was significantly higher than during QW, REM and SWS states (Figure 1C, P<0.01, P<0.001). The HR during QW, REM and SWS showed no significant difference between each other (Figure 1C, QW:REM, P = 0.956; QW:SWS, P = 0.098; REM:SWS, P = 0.215).

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