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Social buffering suppresses fear-associated activation of the lateral amygdala in male rats: behavioral and neurophysiological evidence.

Fuzzo F, Matsumoto J, Kiyokawa Y, Takeuchi Y, Ono T, Nishijo H - Front Neurosci (2015)

Bottom Line: Although these findings suggest that the presence of a conspecific animal suppresses neural activity in the LA, direct neurophysiological evidence of suppressed activity in the LA during social buffering is still lacking.The presence of a conspecific animal significantly decreased the mean peak amplitudes of auditory evoked field potentials, gamma oscillations (25-75 Hz) and high frequency oscillations (100-300 Hz) in the LA.The results provide the first electrophysiological evidence that social buffering suppresses CS-induced activation in the LA, which consequently reduces conditioned fear responses.

View Article: PubMed Central - PubMed

Affiliation: System Emotional Science, University of Toyama Sugitani, Toyama, Japan.

ABSTRACT
In social mammals, the presence of an affiliative conspecific reduces stress responses, a phenomenon referred to as "social buffering."In a previous study, we found that the presence of a conspecific animal ameliorated a variety of stress responses to an aversive conditioned stimulus (CS), including freezing and Fos expression in the lateral amygdala (LA) of male rats. Although these findings suggest that the presence of a conspecific animal suppresses neural activity in the LA, direct neurophysiological evidence of suppressed activity in the LA during social buffering is still lacking. In the present study, we analyzed freezing behavior and local field potentials in the LA of fear-conditioned rats in response to the CS, in the presence or absence of a conspecific. After auditory aversive conditioning, the CS was presented to the conditioned rats in the presence or absence of a conspecific animal, on 2 successive days. The presence of a conspecific animal significantly decreased the mean peak amplitudes of auditory evoked field potentials, gamma oscillations (25-75 Hz) and high frequency oscillations (100-300 Hz) in the LA. Furthermore, magnitudes of these neural responses positively correlated with freezing duration of the fear-conditioned rats. The results provide the first electrophysiological evidence that social buffering suppresses CS-induced activation in the LA, which consequently reduces conditioned fear responses.

No MeSH data available.


Related in: MedlinePlus

Reduction of gamma and high frequency (HF) oscillations after the CS in the Social condition in the second fear-expression test. (A,B) Averaged event-related spectral perturbations (ERSPs) in the Alone (A) and the Social (B) conditions. The dotted lines indicate CS onset. Each ERSP value was corrected for a log power spectrum of the −50–0 ms pre-tone period (in dB). (C,D) The time courses of averaged ERSP of gamma (C) and HF (D) oscillations. The red and blue solid lines indicate the mean ERSPs in the Alone and Social conditions, respectively. The corresponding translucent areas indicate the SEMs. The dotted line indicates the CS onset. Yellow bars indicate the latency windows in which there were significant differences between the conditions (P < 0.05, simple main effect analysis). (E,F) Comparison of power changes after the CS in gamma (E) and HF (F) ranges between the conditions. *P < 0.05, Wilcoxon rank-sum test. (G) Locations of the electrodes recording local oscillations in bipolar measurement. Open and filled circles indicate positive and negative poles, respectively. Other conventions are the same as those of Figure 2C.
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Figure 3: Reduction of gamma and high frequency (HF) oscillations after the CS in the Social condition in the second fear-expression test. (A,B) Averaged event-related spectral perturbations (ERSPs) in the Alone (A) and the Social (B) conditions. The dotted lines indicate CS onset. Each ERSP value was corrected for a log power spectrum of the −50–0 ms pre-tone period (in dB). (C,D) The time courses of averaged ERSP of gamma (C) and HF (D) oscillations. The red and blue solid lines indicate the mean ERSPs in the Alone and Social conditions, respectively. The corresponding translucent areas indicate the SEMs. The dotted line indicates the CS onset. Yellow bars indicate the latency windows in which there were significant differences between the conditions (P < 0.05, simple main effect analysis). (E,F) Comparison of power changes after the CS in gamma (E) and HF (F) ranges between the conditions. *P < 0.05, Wilcoxon rank-sum test. (G) Locations of the electrodes recording local oscillations in bipolar measurement. Open and filled circles indicate positive and negative poles, respectively. Other conventions are the same as those of Figure 2C.

Mentions: ERSPs recorded during the presentation of 20 CS in the second fear-expression test were analyzed. Figure 3 shows the grand averaged ERSPs across all rats in the Alone (Figure 3A) and Social (Figure 3B) conditions. Gamma and HF oscillation was more prominent after CS onset in the Alone compared with the Social condition. Response latencies in the two frequency bands were estimated by analyzing at what point after CS onset differences in ERSP values between the two conditions became significant (Figures 3C,D). The first significant differences between the two conditions were noted 28 ms after CS onset in both gamma (simple main effect analysis, P < 0.05) and HF (simple main effect analysis, P < 0.05) bands. Tip locations of the bipolar electrodes recording ERSPs are shown in Figure 3G.


Social buffering suppresses fear-associated activation of the lateral amygdala in male rats: behavioral and neurophysiological evidence.

Fuzzo F, Matsumoto J, Kiyokawa Y, Takeuchi Y, Ono T, Nishijo H - Front Neurosci (2015)

Reduction of gamma and high frequency (HF) oscillations after the CS in the Social condition in the second fear-expression test. (A,B) Averaged event-related spectral perturbations (ERSPs) in the Alone (A) and the Social (B) conditions. The dotted lines indicate CS onset. Each ERSP value was corrected for a log power spectrum of the −50–0 ms pre-tone period (in dB). (C,D) The time courses of averaged ERSP of gamma (C) and HF (D) oscillations. The red and blue solid lines indicate the mean ERSPs in the Alone and Social conditions, respectively. The corresponding translucent areas indicate the SEMs. The dotted line indicates the CS onset. Yellow bars indicate the latency windows in which there were significant differences between the conditions (P < 0.05, simple main effect analysis). (E,F) Comparison of power changes after the CS in gamma (E) and HF (F) ranges between the conditions. *P < 0.05, Wilcoxon rank-sum test. (G) Locations of the electrodes recording local oscillations in bipolar measurement. Open and filled circles indicate positive and negative poles, respectively. Other conventions are the same as those of Figure 2C.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4373252&req=5

Figure 3: Reduction of gamma and high frequency (HF) oscillations after the CS in the Social condition in the second fear-expression test. (A,B) Averaged event-related spectral perturbations (ERSPs) in the Alone (A) and the Social (B) conditions. The dotted lines indicate CS onset. Each ERSP value was corrected for a log power spectrum of the −50–0 ms pre-tone period (in dB). (C,D) The time courses of averaged ERSP of gamma (C) and HF (D) oscillations. The red and blue solid lines indicate the mean ERSPs in the Alone and Social conditions, respectively. The corresponding translucent areas indicate the SEMs. The dotted line indicates the CS onset. Yellow bars indicate the latency windows in which there were significant differences between the conditions (P < 0.05, simple main effect analysis). (E,F) Comparison of power changes after the CS in gamma (E) and HF (F) ranges between the conditions. *P < 0.05, Wilcoxon rank-sum test. (G) Locations of the electrodes recording local oscillations in bipolar measurement. Open and filled circles indicate positive and negative poles, respectively. Other conventions are the same as those of Figure 2C.
Mentions: ERSPs recorded during the presentation of 20 CS in the second fear-expression test were analyzed. Figure 3 shows the grand averaged ERSPs across all rats in the Alone (Figure 3A) and Social (Figure 3B) conditions. Gamma and HF oscillation was more prominent after CS onset in the Alone compared with the Social condition. Response latencies in the two frequency bands were estimated by analyzing at what point after CS onset differences in ERSP values between the two conditions became significant (Figures 3C,D). The first significant differences between the two conditions were noted 28 ms after CS onset in both gamma (simple main effect analysis, P < 0.05) and HF (simple main effect analysis, P < 0.05) bands. Tip locations of the bipolar electrodes recording ERSPs are shown in Figure 3G.

Bottom Line: Although these findings suggest that the presence of a conspecific animal suppresses neural activity in the LA, direct neurophysiological evidence of suppressed activity in the LA during social buffering is still lacking.The presence of a conspecific animal significantly decreased the mean peak amplitudes of auditory evoked field potentials, gamma oscillations (25-75 Hz) and high frequency oscillations (100-300 Hz) in the LA.The results provide the first electrophysiological evidence that social buffering suppresses CS-induced activation in the LA, which consequently reduces conditioned fear responses.

View Article: PubMed Central - PubMed

Affiliation: System Emotional Science, University of Toyama Sugitani, Toyama, Japan.

ABSTRACT
In social mammals, the presence of an affiliative conspecific reduces stress responses, a phenomenon referred to as "social buffering."In a previous study, we found that the presence of a conspecific animal ameliorated a variety of stress responses to an aversive conditioned stimulus (CS), including freezing and Fos expression in the lateral amygdala (LA) of male rats. Although these findings suggest that the presence of a conspecific animal suppresses neural activity in the LA, direct neurophysiological evidence of suppressed activity in the LA during social buffering is still lacking. In the present study, we analyzed freezing behavior and local field potentials in the LA of fear-conditioned rats in response to the CS, in the presence or absence of a conspecific. After auditory aversive conditioning, the CS was presented to the conditioned rats in the presence or absence of a conspecific animal, on 2 successive days. The presence of a conspecific animal significantly decreased the mean peak amplitudes of auditory evoked field potentials, gamma oscillations (25-75 Hz) and high frequency oscillations (100-300 Hz) in the LA. Furthermore, magnitudes of these neural responses positively correlated with freezing duration of the fear-conditioned rats. The results provide the first electrophysiological evidence that social buffering suppresses CS-induced activation in the LA, which consequently reduces conditioned fear responses.

No MeSH data available.


Related in: MedlinePlus