Characterization of stress-induced suppression of long-term potentiation in the hippocampal CA1 field of freely moving rats

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

doi:10.1016/j.brainres.2008.06.004

Cited by 22 publications

(11 citation statements)

References 19 publications

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“…Freezing behavior in each rat during extinction retrieval inversely correlated with the synaptic response evaluated by AUC of the PSA (P < 0.01). 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).…”

Section: Discussionsupporting

confidence: 88%

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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Section: Discussionsupporting

confidence: 88%

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

et al. 2013

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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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“…Synaptically evoked responses recorded extracellularly in the various hippocampal areas were usually not affected by corticosterone or stress (Pavlides et al, 1996;Bramham et al, 1998;Zhou et al, 2000;Yamada et al, 2003;Chen et al, 2010), although enhancements (Avital et al, 2006; or reduced activity (Hirata et al, 2008) were reported in a few studies. Corticosteroid actions on excitatory or inhibitory transmission are restricted to a limited number of synapses and thus not discernible at a more general level, similar to what has been found after learning (Whitlock et al, 2006).…”

Section: Mr + Gr Mr Adxmentioning

confidence: 99%

“…Numerous studies have shown that the induction of LTP in the CA1 hippocampal area is severely hampered several hours after administration of corticosterone in vitro or in vivo or after exposure to stress, especially stress of an uncontrollable nature (Foy et al, 1987;Shors et al, 1989;Diamond et al, 1992;Shors and Thompson, 1992;Diamond and Rose, 1994;Kim et al, 1996Kim et al, , 2001Zhou et al, 2000;Xiong et al, 2004;Hirata et al, 2008Hirata et al, , 2009Li et al, 2008;Yang et al, 2008a;Cazakoff and Howland, 2010;Ryan et al, 2010;Ooishi et al, 2012; for review, see Kim and Diamond, 2002) (Supplemental Table II). This is a GR-dependent phenomenon (Pavlides et al, 1996); depends on NMDA-receptor mediated transmission (Kim et al, 1996); depends on phosphatidylinositol 3-kinase (Yang et al, 2008b); requires the basolateral amygdala, particularly ERK1/2 phosphorylation (Kim et al, 2001;Yang et al, 2008a); and can be rescued by estradiol 918 administration in vitro (Ooishi et al, 2012).…”

Section: B Slow Modulation Of Synaptic Plasticitymentioning

confidence: 99%

Unraveling the Time Domains of Corticosteroid Hormone Influences on Brain Activity: Rapid, Slow, and Chronic Modes

Joëls

Sarabdjitsingh

Karst

2012

Pharmacological Reviews

375

300

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Characterization of stress-induced suppression of long-term potentiation in the hippocampal CA1 field of freely moving rats

Cited by 22 publications

References 19 publications

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

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

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

Unraveling the Time Domains of Corticosteroid Hormone Influences on Brain Activity: Rapid, Slow, and Chronic Modes

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