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Elevated emotional contagion in a mouse model of Alzheimer ’ s disease is associated with increased synchronization in the insula and amygdala

View Article: PubMed Central - PubMed

ABSTRACT

Emotional contagion, a primitive form of empathy, is heightened in patients with Alzheimer’s disease (AD); however, the mechanism underlying this attribute has not been thoroughly elucidated. In this study, observational fear conditioning was performed to measure emotional contagion levels in a mouse model of AD. Simultaneous recording of local field potentials in the bilateral anterior insula, basolateral amygdala, anterior cingulate cortex, and retrosplenial cortex was also conducted to investigate related brain network changes. Consistent with the results obtained with AD patients, 11-month-old AD model mice exhibited significantly higher freezing levels in observational fear conditioning, indicating elevated emotional contagion compared to age-matched wild-type mice. Furthermore, the left anterior insula and right basolateral amygdala of 11-months-old AD model mice indicated sustained increases in synchronization when they observed the suffering of conspecifics. These changes did not appear in other age groups or wild-type controls. Additionally, the amyloid plaque burden within the anterior insula was significantly correlated with the freezing levels in observational fear conditioning. Taken together, this study reveals increased and sustained network synchrony between the anterior insula and basolateral amygdala, which comprise a salience network in humans, as a potential mechanism for elevated emotional contagion in a mouse model of AD.

No MeSH data available.


Changes in the network correlation of Tg-11 mice remained longer during the conditioning session in OFC.(A) Schematic drawing of the divided sessions for analysis. Qr: Quarter. (B,C) Cross-correlation matrix during the habituation and 4 quarters of Wt-11 and Tg-11 mice (Wt-11: n = 7; Tg-11: n = 10). (D) Matrix dissimilarity was calculated based on the Euclidean distance (see Methods) from the habituation matrix to each quarter matrix. The dotted lines represent the trend lines of the dynamics of each matrix. There was no significant relationship between the two groups (r = −0.772 P = 0.228, Pearson’s correlation).
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f3: Changes in the network correlation of Tg-11 mice remained longer during the conditioning session in OFC.(A) Schematic drawing of the divided sessions for analysis. Qr: Quarter. (B,C) Cross-correlation matrix during the habituation and 4 quarters of Wt-11 and Tg-11 mice (Wt-11: n = 7; Tg-11: n = 10). (D) Matrix dissimilarity was calculated based on the Euclidean distance (see Methods) from the habituation matrix to each quarter matrix. The dotted lines represent the trend lines of the dynamics of each matrix. There was no significant relationship between the two groups (r = −0.772 P = 0.228, Pearson’s correlation).

Mentions: To investigate changes of the correlation matrix over time, the conditioning period was divided into four quarters (Fig. 3A). During the first quarter, the matrices of both Wt-11 and Tg-11 mice displayed general increases in network correlation. However, whereas the changes of Tg mice increased in subsequent quarters (Fig. 3C), those of Wt mice returned to the initial state (Fig. 3B). To quantify this result, matrix dissimilarity from the habituation matrix to each quarter matrix was measured. The dissimilarity index of Tg mice remained elevated over time, whereas that of Wt mice decreased (Fig. 3D). There was no correlation between the matrix dynamics of the two groups (r = −0.772, P = 0.228).


Elevated emotional contagion in a mouse model of Alzheimer ’ s disease is associated with increased synchronization in the insula and amygdala
Changes in the network correlation of Tg-11 mice remained longer during the conditioning session in OFC.(A) Schematic drawing of the divided sessions for analysis. Qr: Quarter. (B,C) Cross-correlation matrix during the habituation and 4 quarters of Wt-11 and Tg-11 mice (Wt-11: n = 7; Tg-11: n = 10). (D) Matrix dissimilarity was calculated based on the Euclidean distance (see Methods) from the habituation matrix to each quarter matrix. The dotted lines represent the trend lines of the dynamics of each matrix. There was no significant relationship between the two groups (r = −0.772 P = 0.228, Pearson’s correlation).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5384199&req=5

f3: Changes in the network correlation of Tg-11 mice remained longer during the conditioning session in OFC.(A) Schematic drawing of the divided sessions for analysis. Qr: Quarter. (B,C) Cross-correlation matrix during the habituation and 4 quarters of Wt-11 and Tg-11 mice (Wt-11: n = 7; Tg-11: n = 10). (D) Matrix dissimilarity was calculated based on the Euclidean distance (see Methods) from the habituation matrix to each quarter matrix. The dotted lines represent the trend lines of the dynamics of each matrix. There was no significant relationship between the two groups (r = −0.772 P = 0.228, Pearson’s correlation).
Mentions: To investigate changes of the correlation matrix over time, the conditioning period was divided into four quarters (Fig. 3A). During the first quarter, the matrices of both Wt-11 and Tg-11 mice displayed general increases in network correlation. However, whereas the changes of Tg mice increased in subsequent quarters (Fig. 3C), those of Wt mice returned to the initial state (Fig. 3B). To quantify this result, matrix dissimilarity from the habituation matrix to each quarter matrix was measured. The dissimilarity index of Tg mice remained elevated over time, whereas that of Wt mice decreased (Fig. 3D). There was no correlation between the matrix dynamics of the two groups (r = −0.772, P = 0.228).

View Article: PubMed Central - PubMed

ABSTRACT

Emotional contagion, a primitive form of empathy, is heightened in patients with Alzheimer’s disease (AD); however, the mechanism underlying this attribute has not been thoroughly elucidated. In this study, observational fear conditioning was performed to measure emotional contagion levels in a mouse model of AD. Simultaneous recording of local field potentials in the bilateral anterior insula, basolateral amygdala, anterior cingulate cortex, and retrosplenial cortex was also conducted to investigate related brain network changes. Consistent with the results obtained with AD patients, 11-month-old AD model mice exhibited significantly higher freezing levels in observational fear conditioning, indicating elevated emotional contagion compared to age-matched wild-type mice. Furthermore, the left anterior insula and right basolateral amygdala of 11-months-old AD model mice indicated sustained increases in synchronization when they observed the suffering of conspecifics. These changes did not appear in other age groups or wild-type controls. Additionally, the amyloid plaque burden within the anterior insula was significantly correlated with the freezing levels in observational fear conditioning. Taken together, this study reveals increased and sustained network synchrony between the anterior insula and basolateral amygdala, which comprise a salience network in humans, as a potential mechanism for elevated emotional contagion in a mouse model of AD.

No MeSH data available.