Claustrum mediates bidirectional and reversible control of stress-induced anxiety responses

Zotero | DOI

Bibliography: Niu, M., Kasai, A., Tanuma, M., Seiriki, K., Igarashi, H., Kuwaki, T., Nagayasu, K., Miyaji, K., Ueno, H., Tanabe, W., Seo, K., Yokoyama, R., Ohkubo, J., Ago, Y., Hayashida, M., Inoue, K., Takada, M., Yamaguchi, S., Nakazawa, T., Kaneko, S., Okuno, H., Yamanaka, A., Hashimoto, H. (2022). Claustrum mediates bidirectional and reversible control of stress-induced anxiety responses. Science Advances, 8(11), eabi6375. https://doi.org/10.1126/sciadv.abi6375

Authors:: Misaki Niu, Atsushi Kasai, Masato Tanuma, Kaoru Seiriki, Hisato Igarashi, Takahiro Kuwaki, Kazuki Nagayasu, Keita Miyaji, Hiroki Ueno, Wataru Tanabe, Kei Seo, Rei Yokoyama, Jin Ohkubo, Yukio Ago, Misuzu Hayashida, Ken-ichi Inoue, Masahiko Takada, Shun Yamaguchi, Takanobu Nakazawa, Shuji Kaneko, Hiroyuki Okuno, Akihiro Yamanaka, Hitoshi Hashimoto

Tags: #Claustrum, #Arousal, #Emotion, #Stress

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The processing of stress responses involves brain-wide communication among cortical and subcortical regions; however, the underlying mechanisms remain elusive. Here, we show that the claustrum (CLA) is crucial for the control of stress-induced anxiety-related behaviors. A combined approach using brain activation mapping and machine learning showed that the CLA activation serves as a reliable marker of exposure to acute stressors. In TRAP2 mice, which allow activity-dependent genetic labeling, chemogenetic activation of the CLA neuronal ensemble tagged by acute social defeat stress (DS) elicited anxiety-related behaviors, whereas silencing of the CLA ensemble attenuated DS-induced anxiety-related behaviors. Moreover, the CLA received strong input from DS-activated basolateral amygdala neurons, and its circuit-selective optogenetic photostimulation temporarily elicited anxiety-related behaviors. Last, silencing of the CLA ensemble during stress exposure increased resistance to chronic DS. The CLA thus bidirectionally controls stress-induced emotional responses, and its inactivation can serve as a preventative strategy to increase stress resilience., Claustrum ensemble regulates stress-induced anxiety responses and stress resilience.

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(29/12/2023, 20:41:15 )

CLA emotion modulation due to functional connections to Basolateral Amygdala (BLA)

“This observation also suggests that the CLA ensemble is functionally and anatomically connected to the BLA and thereby modulates emotional processes.” (Niu et al., 2022, p. 7)

CLA emotion control of stress/anxiety

“the claustrum (CLA) is crucial for the control of stress-induced anxiety-related behaviors” (Niu et al., 2022, p. 1)

“The present study demonstrates that the CLA is crucially involved in stress-induced neurobehavioral changes, in which manipulation of the stress-responsive neuronal ensemble bidirectionally controls anxiety-related behavior, as activation augments anxiety-related behaviors and inactivation normalizes them” (Niu et al., 2022, p. 7)

Basolateral Amygdala (BLA) (Niu et al., 2022, p. 7)

CLA activation increases Dopamine and Noradrenalin in mPFC

“chemogenetic activation of CLA neurons increased dopamine and noradrenaline release in the mPFC, and blockade of dopamine and noradrenaline signaling attenuated anxiety-related behaviors” (Niu et al., 2022, p. 7)

“It is well known that the Basolateral Amygdala (BLA) is an integrative hub for regulating affective behaviors”

(Niu et al., 2022, p. 7)

“Imaging studies in the human amygdala/CLA region (the CLA extending into the amygdala) have shown that aversive stimuli activated this region” (Niu et al., 2022, p. 7)

“Optogenetic activation of the anterior BLA neurons evoked negative emotional behavior (disrupting reward-seeking behaviors), while that of the posterior BLA neurons induced positive effects (30). This suggests that the CLA ensemble plays a key role downstream of the anterior BLA, and thus, activation (or inactivation) of this pathway can evoke (or attenuate) anxiety-related behaviors.” (Niu et al., 2022, p. 7)

“As activation of the CLA ensemble caused anxiety-related behaviors (Fig. 2), silencing of the CLA ensemble may reduce anxiety in mice during DS, lowering the experience of social defeat.” (Niu et al., 2022, p. 7)

[[CLA connections]]

“The main projection of the CLA extends to the cortices, such as the frontal cortex, and also to the BLA (25, 26). Therefore, although further experiments are needed, a stress-responsive CLA ensemble may affect LC activity via the BLA-central amygdala circuit. In addition, CLA-to-cortical projections inhibit the prefrontal cortex’s activity (26, 37). The PFC also has direct and indirect connections to the LC, VTA, and amygdala and can regulate its own catecholamine inputs (27). Under psychological stress conditions, stress-responsive CLA ensemble may impair this PFC regulation of catecholamine and/or weaken the BLA inhibition from mPFC neurons (38–40).” (Niu et al., 2022, p. 7)

“We found that CLA ensemble activated by aversive stimuli” CLA salience

“Salient sensory stimuli increase dopamine neuron activity and dopamine release (45). The catecholamine system in the PFC is involved in motivational salience (46). We found that CLA ensemble activated by aversive stimuli increased the dopamine and noradrenaline levels in the PFC, followed by the emergence of anxiety-related behaviors (fig. S5). These data imply that CLA activation may be involved in salient information processing in the open arms of the elevated plus maze, leading to enhanced vigilance” (Niu et al., 2022, p. 7)

“In the present study, we showed that chemogenetic silencing of the CLA neuronal ensemble attenuated the depression-like behavior caused by chronic DS (Fig. 4)” (Niu et al., 2022, p. 8)

“In this study, the impairment in social interaction and anhedonia (reduced sucrose preference) was significantly normalized; however, results in the elevated plus maze test and forced swimming tests were not altered by CLA inhibition” (Niu et al., 2022, p. 8)

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