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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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Instant heart rate responses to handling and novel environment exposures.(A) Illustration of the handling method: cup handling [38] (left) and two examples of instant HR response to handling (right). The red bars indicate the duration of handling (49 seconds and 37 seconds, respectively). (B) Instant HR responses of an individual mouse during repeated exposures to a novel environment (left panels) and illustration of a novel environment (right). The blue vertical line indicates the start of stage-I; the red vertical line indicates the end of stage-I; the green vertical line indicates the end of the novel environment exposure. (C) The duration of stage-I during repeated novel environment exposures. Error bars, s.e.m.; n = 7; *P<0.05, **P<0.01, one-way repeated measures ANOVA and Tukey post hoc test.
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pone-0063590-g002: Instant heart rate responses to handling and novel environment exposures.(A) Illustration of the handling method: cup handling [38] (left) and two examples of instant HR response to handling (right). The red bars indicate the duration of handling (49 seconds and 37 seconds, respectively). (B) Instant HR responses of an individual mouse during repeated exposures to a novel environment (left panels) and illustration of a novel environment (right). The blue vertical line indicates the start of stage-I; the red vertical line indicates the end of stage-I; the green vertical line indicates the end of the novel environment exposure. (C) The duration of stage-I during repeated novel environment exposures. Error bars, s.e.m.; n = 7; *P<0.05, **P<0.01, one-way repeated measures ANOVA and Tukey post hoc test.

Mentions: Typically, prior to fear conditioning experiments, mice are picked up from home cages and then placed into a conditioning chamber. This standard practice can represent a dramatic change in physical and emotional states for animals and was usually repeated prior to fear conditioning as a habituation procedure. We asked how heart rate (HR) and heart rate variability (HRV) might change by this handling procedure. We found robust increase in HR at the onset of picking-up the mice from the home cages by the experimenter (Figure 2A). We noticed that in addition to HR increase, placing mice in hand also caused a sustained reduction of HRV (red bar in Figure 2A). This HRV reduction phase was correlated with the duration of time during which mice stayed in hand (see examples in Fig. 2A, two holding periods: 49 seconds for the first epoch, and 37 seconds for the second epoch, respectively). However, once the mouse was placed back in the home cage, this reduced HRV phase quickly returned to the more variable base level. At the same time, HR would also reverse back to the base rate. This transient hand holding effect on HRV were consistently observed despite repeated handling of mice for many days (two sessions of 5 minutes handling each day for 5 days). This suggests that hand handling is a transient emotional state, correlated with the time duration of mice staying in experimenter’s hands.


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)

Instant heart rate responses to handling and novel environment exposures.(A) Illustration of the handling method: cup handling [38] (left) and two examples of instant HR response to handling (right). The red bars indicate the duration of handling (49 seconds and 37 seconds, respectively). (B) Instant HR responses of an individual mouse during repeated exposures to a novel environment (left panels) and illustration of a novel environment (right). The blue vertical line indicates the start of stage-I; the red vertical line indicates the end of stage-I; the green vertical line indicates the end of the novel environment exposure. (C) The duration of stage-I during repeated novel environment exposures. Error bars, s.e.m.; n = 7; *P<0.05, **P<0.01, one-way repeated measures ANOVA and Tukey post hoc test.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3646801&req=5

pone-0063590-g002: Instant heart rate responses to handling and novel environment exposures.(A) Illustration of the handling method: cup handling [38] (left) and two examples of instant HR response to handling (right). The red bars indicate the duration of handling (49 seconds and 37 seconds, respectively). (B) Instant HR responses of an individual mouse during repeated exposures to a novel environment (left panels) and illustration of a novel environment (right). The blue vertical line indicates the start of stage-I; the red vertical line indicates the end of stage-I; the green vertical line indicates the end of the novel environment exposure. (C) The duration of stage-I during repeated novel environment exposures. Error bars, s.e.m.; n = 7; *P<0.05, **P<0.01, one-way repeated measures ANOVA and Tukey post hoc test.
Mentions: Typically, prior to fear conditioning experiments, mice are picked up from home cages and then placed into a conditioning chamber. This standard practice can represent a dramatic change in physical and emotional states for animals and was usually repeated prior to fear conditioning as a habituation procedure. We asked how heart rate (HR) and heart rate variability (HRV) might change by this handling procedure. We found robust increase in HR at the onset of picking-up the mice from the home cages by the experimenter (Figure 2A). We noticed that in addition to HR increase, placing mice in hand also caused a sustained reduction of HRV (red bar in Figure 2A). This HRV reduction phase was correlated with the duration of time during which mice stayed in hand (see examples in Fig. 2A, two holding periods: 49 seconds for the first epoch, and 37 seconds for the second epoch, respectively). However, once the mouse was placed back in the home cage, this reduced HRV phase quickly returned to the more variable base level. At the same time, HR would also reverse back to the base rate. This transient hand holding effect on HRV were consistently observed despite repeated handling of mice for many days (two sessions of 5 minutes handling each day for 5 days). This suggests that hand handling is a transient emotional state, correlated with the time duration of mice staying in experimenter’s hands.

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
Related in: MedlinePlus