Early postnatal stress alters the 5-HTergic modulation to emotional stress at postadolescent periods of rats

Matsumoto, Machiko; Higuchi, Kasane; Togashi, Hiroko; Koseki, Hiroyo; Yamaguchi, Taku; Kanno, Manabu; Yoshioka, Mitsuhiro

doi:10.1002/hipo.20100

Cited by 46 publications

(20 citation statements)

References 36 publications

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“…Consistent with previous studies (4,18), fear-related freezing behavior was markedly reduced during CFC retention in the 2wFS group. The low levels of freezing unlikely resulted from deficits in the acquisition of fear conditioning because the expression of freezing immediately after FS conditioning was similar to non-FS controls.…”

Section: Discussionsupporting

confidence: 92%

“…Based on these findings, the authors suggested that long-term deficits in amygdala function impair fear memory consolidation (17). Interestingly, we also observed that early postnatally stressed animals that received aversive footshock (FS) stimuli during postnatal days 14 to 18 (2nd week FS [2wFS] group) exhibited a marked reduction in freezing behavior during the CFC retention session (4,18). Furthermore, decreases in synaptic transmission in the CA1 field during the CFC retention session did not occur in the 2wFS group (4).…”

Section: Introductionmentioning

confidence: 74%

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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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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 74%

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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“…LTP was induced by high-frequency stimulation (HFS: tetanus, 10 trains of stimuli, 10 pulses at 100 Hz, 10-s intertrain intervals) with the same stimulation intensity used for baseline recordings. Tetanus was given at the same intensity as that of the test stimulus (29,30).…”

Section: Electrophysiological Experimentsmentioning

confidence: 99%

Metaplastic Regulation of the Median Raphe Nucleus via Serotonin 5-HT1A Receptor on Hippocampal Synaptic Plasticity Is Associated With Gender-Specific Emotional Expression in Rats

et al. 2014

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Abstract. Gender differences in psychiatric disorders are considered to be associated with the serotonergic (5-HTergic) system; however the underlying mechanisms have not been clearly elucidated. In this study, possible involvement of the median raphe nucleus (MRN)-hippocampus 5-HTergic system in gender-specific emotional regulation was investigated, focusing on synaptic plasticity in rats. A behavioral study using a contextual fear conditioning (CFC) paradigm showed that the females exhibited low anxiety-like behavior. Extracellular 5-HT levels in the hippocampus were increased by CFC only in the males. Long-term potentiation (LTP) in the hippocampal CA1 field was suppressed after CFC in the males, which was mimicked by the synaptic response to MRN electrical stimulation. In the MRN, 5-HT immunoreactive cells significantly increased in the females compared with those in the males. Pretreatment with the 5-HT 1A receptor agonists tandospirone (10 mg/kg, i.p.) and 8-OH DPAT (3 mg/kg, i.p.) significantly suppressed LTP induction in the males. Synaptic responses to CFC and 5-HT 1A receptor interventions were not observed in the females. These results suggest that the metaplastic 5-HTergic mechanism via 5-HT 1A receptors in the MRN-hippocampus pathway is a key component for gender-specific emotional regulation and may be a cause of psychiatric disorders associated with vulnerability or resistance to emotional stress.

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“…They showed that fear-related freezing behavior observed during exposure to contextual fear conditioning was markedly attenuated in the mouse exposed to aversive stimulus (foot-shock) at the postnatal period of the second week, but not of the third week. The second postnatal week may be the "critical period" for establishing proper behavioral responses to emotional stress in adult rats (Matsumoto et al, 2005). Our present results suggested that the "critical period" should be envisioned for mice, involving the adaptation to emotional stress in the adolescent mice.…”

Section: Discussionmentioning

confidence: 61%

“…7) It is interesting to note that when the stress was applied immediately after weaning, 3 weeks after birth, the mice did not show any changes in the emotion-related behavior during the adolescent period. Lately, Matsumoto et al 9) reported the alteration of the neuronal modulation to emotional stress by early postnatal stress during the postadolescent periods of rats. They showed that fear-related freezing behavior observed during exposure to contextual fear conditioning was markedly attenuated in the mouse exposed to aversive stimulus (foot-shock) at the postnatal period of the second week, but not of the third week.…”

Section: Discussionmentioning

confidence: 99%

Effects of Perinatal Stress on the Emotion-Related Behavior of the Adolescent Mouse

Tokumo

Hanabusa

Nishino

2006

Biological & Pharmaceutical Bulletin

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We examined the effects of perinatal stress on the emotion-related behavior of the mouse during their adolescent period. Firstly, we applied the sound noise and/or the forced swim stress to the maternal pregnant mice in the pregnant mice at 10 to 18 d gestation. The stress applied during the fetal period did affect neither the spontaneous locomotor activity of the offspring mice in a new environment at an age of 4 weeks, nor those soundinduced changes in the locomotor activity. Secondly, we applied the stress to the neonatal mouse during the late lactation period, 14 to 18 d after birth. The mice that underwent the forced swim stress accompanied by the sound noise stress showed a significant reduction of the locomotor activity. On the other hand, the mice that underwent the forced swim stress during the lactation period showed a significant increase in the locomotor activity after the stimulation by the sound noise. Lastly, we applied the stress to the neonatal mouse immediately after the weaning period, 21 to 25 d after birth. The spontaneous locomotor activity of the mice was not changed compared to that of the non-stressed group. Thus, it was found that the stress applied to the mice during the lactation period, thought to be the critical period of mouse brain development, selectively influenced the emotion-related behavior in the subsequent adolescent period. These results suggested that second postnatal week may be the critical period for establishing proper behavioral responses to emotional stress in the adolescent mouse.

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Early postnatal stress alters the 5-HTergic modulation to emotional stress at postadolescent periods of rats

Cited by 46 publications

References 36 publications

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

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

Metaplastic Regulation of the Median Raphe Nucleus via Serotonin 5-HT1A Receptor on Hippocampal Synaptic Plasticity Is Associated With Gender-Specific Emotional Expression in Rats

Effects of Perinatal Stress on the Emotion-Related Behavior of the Adolescent Mouse

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