Possible relationship between the stress‐induced synaptic response and metaplasticity in the hippocampal CA1 field of freely moving rats

Hirata, Riki; Matsumoto, Machiko; Judo, C.; Yamaguchi, Taku; Izumi, Tohru; Yoshioka, Mitsuhiro; Togashi, Hiroko

doi:10.1002/syn.20631

Cited by 25 publications

(13 citation statements)

References 43 publications

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“…On the other hand, CFC stress robustly induced c-Fos expression in all DRN subdivisions examined, and this was significantly suppressed by diazepam. Considering higher plasma corticosterone concentrations induced by CFC stress than OF stress (Hirata et al, 2008;Hirata et al, 2009), the different neuronal responses between the two tests might be related to different types and intensities of stressors. While exposing animals to an OF arena drives the motivation of novelty-seeking behavior on one hand, it also increases the anxiety on the other hand, because of the novelty of unfamiliar environments (Gray and McNaughton, 2003;Padilla et al, 2010;Molander et al, 2011).…”

Section: Discussionmentioning

confidence: 99%

Distinct Neurochemical and Functional Properties of GAD67-Containing 5-HT Neurons in the Rat Dorsal Raphe Nucleus

Shikanai

Yoshida²,

Konno

et al. 2012

J. Neurosci.

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The serotonergic (5-HTergic) system arising from the dorsal raphe nucleus (DRN) is implicated in various physiological and behavioral processes, including stress responses. The DRN is comprised of several subnuclei, serving specific functions with distinct afferent and efferent connections. Furthermore, subsets of 5-HTergic neurons are known to coexpress other transmitters, including GABA, glutamate, or neuropeptides, thereby generating further heterogeneity. However, despite the growing evidence for functional variations among DRN subnuclei, relatively little is known about how they map onto neurochemical diversity of 5-HTergic neurons. In the present study, we characterized functional properties of GAD67-expressing 5-HTergic neurons (5-HT/GAD67 neurons) in the rat DRN, and compared with those of neurons expressing 5-HTergic molecules (5-HT neurons) or GAD67 alone. While 5-HT/GAD67 neurons were absent in the dorsomedial (DRD) or ventromedial (DRV) parts of the DRN, they were selectively distributed in the lateral wing of the DRN (DRL), constituting 12% of the total DRL neurons. They expressed plasmalemmal GABA transporter 1, but lacked vesicular inhibitory amino acid transporter. By using whole-cell patch-clamp recording, we found that 5-HT/GAD67 neurons had lower input resistance and firing frequency than 5-HT neurons. As revealed by c-Fos immunohistochemistry, neurons in the DRL, particularly 5-HT/GAD67 neurons, showed higher responsiveness to exposure to an open field arena than those in the DRD and DRV. By contrast, exposure to contextual fear conditioning stress showed no such regional differences. These findings indicate that 5-HT/GAD67 neurons constitute a unique neuronal population with distinctive neurochemical and electrophysiological properties and high responsiveness to innocuous stressor.

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Section: Discussionmentioning

confidence: 99%

Distinct Neurochemical and Functional Properties of GAD67-Containing 5-HT Neurons in the Rat Dorsal Raphe Nucleus

Shikanai

Yoshida²,

Konno

et al. 2012

J. Neurosci.

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“…These synaptic changes mimicked those induced by LFS prior to tetanus; LFS application prior to tetanus caused enhancement of LTP in DG, whereas it suppressed LTP in the CA1 field (20). Synaptic metaplasticity in the CA1 field (i.e., LTP suppression by LFS application prior to tetanus) is considered to serve as a cellular mechanism of stress experience-dependent fear memory (20,31,35). Therefore, LFS-primed synaptic changes in the hippocampal subregions appear to reflect one aspect of responses to CFS.…”

Section: Discussionmentioning

confidence: 65%

“…CA1 field was impaired by BLA activation (7,32) and CFS (33,34), the present data strengthen the findings that stress exposure, in addition to BLA activation, has opposing effects on synaptic plasticity in a hippocampal subregion-specific manner. These synaptic changes mimicked those induced by LFS prior to tetanus; LFS application prior to tetanus caused enhancement of LTP in DG, whereas it suppressed LTP in the CA1 field (20). Synaptic metaplasticity in the CA1 field (i.e., LTP suppression by LFS application prior to tetanus) is considered to serve as a cellular mechanism of stress experience-dependent fear memory (20,31,35).…”

Section: Discussionmentioning

confidence: 81%

“…We first examined the effects of BLA activation or exposure to conditioned fear stress (CFS) on LTP in mPFC, compared with those in the hippocampal DG subregion. On the basis of previous reports that synaptic metaplasticity, i.e., LTP suppression, by LFS prior to tetanus in CA1 is regulated by BLA (19,20), we next examined the possible involvement of BLA modulation in LFS-primed LTP in mPFC. Finally, we investigated the effects of BLA activation on synaptic changes responsible for extinction retrieval of context-dependent fear memory.…”

Section: Synaptic Modulation Via Basolateral Amygdala On the Rat Hippmentioning

confidence: 99%

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Synaptic Modulation via Basolateral Amygdala on the Rat Hippocampus–Medial Prefrontal Cortex Pathway in Fear Extinction

et al. 2013

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Abstract. The present study elucidated the functional role of modulatory effects of basolateral amygdala (BLA) on synaptic transmission in the rat hippocampus-medial prefrontal cortex (mPFC) pathway, compared with the hippocampal dentate gyrus (DG). Exposure to conditioned fear stress (CFS) or prior BLA activation enhanced tetanus-induced long-term potentiation (LTP) in DG. A similar synaptic response was found by low frequency stimulation (LFS) prior to tetanus. In mPFC, they did not affect LTP, but prior BLA activation, as well as pretreatment with the Nmethyl-d-aspartate (NMDA)-receptor antagonist MK-801 (0.1 mg/kg, i.p.), suppressed LFSprimed LTP. This BLA-mediated synaptic pattern was mimicked by synaptic changes observed in the fear extinction process; prior BLA activation suppressed the synaptic potentiation responsible for extinction retrieval and attenuated decreases in fear-related freezing behavior. These data suggest that LFS-primed LTP in mPFC is related to the neural basis of extinction. Extinctionrelated synaptic potentiation did not occur in a juvenile stress model that exhibited extinction deficit. In addition, LFS-primed LTP was suppressed in this model, which was reversed by the NMDA-receptor agonist d-cycloserine (15 mg/kg, i.p.). These findings suggest that modulatory effects of BLA on synaptic function in the hippocampus-mPFC pathway play a significant role in fear extinction in rats.

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“…The suppression of LTP in the CA1 field was caused not only by stress paradigms but also by low-frequency stimulation (LFS) prior to LTP-inducing high frequency stimulation (tetanus), termed metaplasticity (7,8). This homosynaptic metaplasticity appears to reflect one aspect of hippocampal function in the mediation of responses to stress because of the similar electrophysiological (9, 10) and neurochemical (11) profiles.…”

Section: Introductionmentioning

confidence: 99%

Possible Modulation of the Amygdala on Metaplasticity Deficits in the Hippocampal CA1 Field in Early Postnatally Stressed Rats

Hiraide¹,

Saito²,

Matsumoto³

et al. 2012

J Pharmacol Sci

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Abstract. Several lines of evidence have shown that early life experiences have a profound impact on fear-related behavior, but the detailed mechanisms are unknown. The present study examined the possible involvement of the amygdala in behavioral deficits associated with fear memory in a juvenile stress model, with a focus on hippocampal synaptic function. Adult rats exposed to footshock (FS) stress during the second postnatal period (2wFS group) exhibited low levels of freezing in response to contextual fear conditioning (CFC). The CFC-induced suppression of longterm potentiation (LTP) in the CA1 field was not found in the 2wFS group. Additionally, synaptic metaplasticity, that is, low-frequency stimulation-induced suppression of subsequent LTP, did not occur in the 2wFS group; instead, LTP was induced. These synaptic changes mimicked the impairment in metaplasticity induced by reversible inactivation of the basolateral amygdala (BLA). Inactivation of the BLA markedly decreased freezing behavior in non-FS controls, similar to the 2wFS group. Furthermore, extracellular signal-regulated kinase activation in the BLA in response to CFC did not occur in the 2wFS group. These findings suggest that early postnatal stress may cause long-term dysfunction of the modulatory effect of the amygdala on hippocampal function associated with fear memory.

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Possible relationship between the stress‐induced synaptic response and metaplasticity in the hippocampal CA1 field of freely moving rats

Cited by 25 publications

References 43 publications

Distinct Neurochemical and Functional Properties of GAD67-Containing 5-HT Neurons in the Rat Dorsal Raphe Nucleus

Distinct Neurochemical and Functional Properties of GAD67-Containing 5-HT Neurons in the Rat Dorsal Raphe Nucleus

Synaptic Modulation via Basolateral Amygdala on the Rat Hippocampus–Medial Prefrontal Cortex Pathway in Fear Extinction

Possible Modulation of the Amygdala on Metaplasticity Deficits in the Hippocampal CA1 Field in Early Postnatally Stressed Rats

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