Role of presynaptic 5-HT1A and 5-HT3 receptors in modulation of synaptic GABA transmission in dissociated rat basolateral amygdala neurons

Koyama, Susumu; Matsumoto, Nozomu; Murakami, Nobuya; Kubo, Chiharu; Nabekura, Junichi; Akaike, Norio

doi:10.1016/s0024-3205(02)02280-4

Cited by 68 publications

(45 citation statements)

References 21 publications

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“…One major concern is the extent to which the 5-HT 2A receptor contributes to serotonergic facilitation of GABA release, given that activation of another serotonin receptor, the 5-HT 3 receptor, has also been shown to facilitate GABA release in dissociated BLA neurons (Koyama et al, 2000(Koyama et al, , 2002. To address this concern, we examined the effect of serotonin in the presence of the 5-HT 2A receptor antagonist alone.…”

Section: -Ht 2a Receptors Mediate Serotonergic Facilitation Of Gaba mentioning

confidence: 99%

“…There may be several reasons why the contribution of the 5-HT 3 receptor to serotonergic facilitation of GABA release is small under our experimental conditions. First, the 5-HT 3 and 5-HT 1 receptors could coexist in the same GABAergic terminals, and activation of the 5-HT 1 receptor could antagonize 5-HT 3 receptor-mediated facilitation of GABA release (Koyama et al, 2002). Thus, the effect of 5-HT 3 receptor activation may not be evident with the 5-HT 1 receptor unantagonized.…”

Section: -Ht 2a Receptors Mediate Serotonergic Facilitation Of Gaba mentioning

confidence: 99%

“…Thus, the effect of 5-HT 3 receptor activation may not be evident with the 5-HT 1 receptor unantagonized. Second, the 5-HT 3 receptor is present only in a subset of GABAergic terminals and the effect of 5-HT 3 receptor activation on GABA release is mainly transient in nature and quickly desensitized (Koyama et al, 2000(Koyama et al, , 2002. To see the effect mediated by the 5-HT 3 receptor, a fast perfusion system (in which the exchange rate of the perfusion is in the millisecond range) was required to apply the 5HT 3 agonist (Koyama et al, 2000(Koyama et al, , 2002.…”

Section: -Ht 2a Receptors Mediate Serotonergic Facilitation Of Gaba mentioning

confidence: 99%

“…Second, the 5-HT 3 receptor is present only in a subset of GABAergic terminals and the effect of 5-HT 3 receptor activation on GABA release is mainly transient in nature and quickly desensitized (Koyama et al, 2000(Koyama et al, , 2002. To see the effect mediated by the 5-HT 3 receptor, a fast perfusion system (in which the exchange rate of the perfusion is in the millisecond range) was required to apply the 5HT 3 agonist (Koyama et al, 2000(Koyama et al, , 2002. Therefore, when serotonin was being applied using our bath perfusion system in which the exchange rate of bath solution is in the range of 1-2 min, a significant amount of the 5-HT 3 receptors may have been desensitized before the agonist reached the effective concentration.…”

Section: -Ht 2a Receptors Mediate Serotonergic Facilitation Of Gaba mentioning

confidence: 99%

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Stress Impairs 5-HT2A Receptor-Mediated Serotonergic Facilitation of GABA Release in Juvenile Rat Basolateral Amygdala

Jiang

Xing

Yang

et al. 2008

Neuropsychopharmacol

130

123

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The occurrence of stress and anxiety disorders has been closely associated with alterations of the amygdala GABAergic system. In these disorders, dysregulation of the serotonergic system, a very important modulator of the amygdala GABAergic system, is also well recognized. The present study, utilizing a learned helplessness stress rat model, was designed to determine whether stress is capable of altering serotonergic modulation of the amygdala GABAergic system. In control rats, administration of 5-HT or a-methyl-5-HT, a 5-HT 2 receptor agonist, to basolateral amygdala (BLA) slices dramatically enhanced frequency and amplitude of spontaneous inhibitory postsynaptic currents (sIPSCs). This effect was blocked by selective 5-HT 2A receptor antagonists while a selective 5-HT 2B receptor agonist and a selective 5-HT 2C receptor agonist were without effect on sIPSCs. Double immunofluorescence labeling demonstrated that the 5-HT 2A receptor is primarily localized to parvalbumin-containing BLA interneurons. Thus, serotonin primarily acts via 5-HT 2A receptors to facilitate BLA GABAergic inhibition. In stressed rats, the 5-HT 2A receptor-mediated facilitative actions were severely impaired. Quantitative RT-PCR and western blot analysis showed that the impairment of 5-HT 2A receptor signaling primarily resulted from receptor downregulation. The stress-induced effect appeared to be specific to 5-HT 2A receptors because stress had no significant impact on other serotonin receptors, as well as histamine H 3 receptor and a 2 adrenoceptor signaling in the BLA. This severe impairment of 5-HT 2A receptor-mediated facilitation of BLA GABAergic inhibition might result in an amygdala circuitry with hyperexcitability, and a lower threshold of activation, and thus be an important mechanism underlying the emergence of stress-associated psychiatric symptoms.

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Section: -Ht 2a Receptors Mediate Serotonergic Facilitation Of Gaba mentioning

confidence: 99%

Section: -Ht 2a Receptors Mediate Serotonergic Facilitation Of Gaba mentioning

confidence: 99%

Section: -Ht 2a Receptors Mediate Serotonergic Facilitation Of Gaba mentioning

confidence: 99%

Section: -Ht 2a Receptors Mediate Serotonergic Facilitation Of Gaba mentioning

confidence: 99%

See 2 more Smart Citations

Stress Impairs 5-HT2A Receptor-Mediated Serotonergic Facilitation of GABA Release in Juvenile Rat Basolateral Amygdala

Jiang

Xing

Yang

et al. 2008

Neuropsychopharmacol

130

123

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“…Some studies found that application of 5-HT1A receptor agonists in the BLA inhibits neuronal excitability and the inhibitory actions of 5-HT on BLA neurons can be prevented by a 5-HT1A receptor antagonist (Cheng et al 1998;Wang et al 1999;Stein et al 2000). Other studies found that 5-HT1A receptor agonists can also suppress GABA interneuron activity in the BLA (Koyama et al 1999;Koyama et al 2002). Exposure to stress can also impact the BLA through desensitization of 5-HT1A autoreceptors (Laaris et al 1997;Lanfumey et al 1999;Gartside et al 2003;Froger et al 2004), likely impairing inhibition of serotonin release at these terminals in the BLA.…”

Section: Dorsal Raphe Nuclei Projections To the Blamentioning

confidence: 99%

Input-specific contributions to valence processing in the amygdala

Correia

Goosens

2016

Learn. Mem.

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Reward and punishment are often thought of as opposing processes: rewards and the environmental cues that predict them elicit approach and consummatory behaviors, while punishments drive aversion and avoidance behaviors. This framework suggests that there may be segregated brain circuits for these valenced behaviors. The basolateral amygdala (BLA) is one brain region that contributes to both types of motivated behavior. Individual neurons in the BLA can favor positive over negative valence, or vice versa, but these neurons are intermingled, showing no anatomical segregation. The amygdala receives inputs from many brain areas and current theories posit that encoding of positive versus negative valence by BLA neurons is determined by the wiring of each neuron. Specifically, many projections from other brain areas that respond to positive and negative valence stimuli and predictive cues project strongly to the BLA and likely contribute to valence processing within the BLA. Here we review three of these areas, the basal forebrain, the dorsal raphe nucleus and the ventral tegmental area, and discuss how these may promote encoding of positive and negative valence within the BLA.The basic desire to seek reward and avoid punishment shapes virtually all of behavior, and the ability to discriminate between "good" and "bad" environmental cues is critical for guiding choices and maximizing survival. Thus, understanding the brain circuits that encode motivated behaviors is important because it contributes to our knowledge of how we learn, and it is also essential for understanding human disorders associated with abnormal processing of reward and danger (i.e., emotional disorders), such as anxiety, depression, addiction, and post-traumatic stress disorder (PTSD).The amygdala is one brain area implicated in motivated behaviors and the basolateral complex of the amygdala (BLA) receives information about diverse environmental stimuli from many brain regions. The BLA is thought to encode the association of predictive stimuli with both aversive and appetitive outcomes (Morrison and Salzman 2010;Barberini et al. 2012). Reward and punishment are reinforcers of opposite valence (positive versus negative), and these reinforcers typically lead to opposing behaviors (approach versus avoidance). Many theories have suggested that appetitive and aversive systems act in opponent fashion (Solomon and Corbit 1974;Daw et al. 2002). However, it is unclear how the BLA contributes to this. We do not yet understand the extent to which aversive and appetitive information is processed in parallel BLA circuits, or whether individual BLA neurons are involved in the regulation of both types of motivated behaviors.In this review, we propose several models by which functional segregation of valence can be achieved in the BLA. These models are based on studies describing how BLA neurons respond to reward and aversive stimuli. We then consider whether three major inputs, known to carry valenced information, support or conflict these models, and also discus...

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The basolateral amygdala γ‐aminobutyric acidergic system in health and disease

Prager

Bergstrom

Wynn

et al. 2015

J of Neuroscience Research

152

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The brain comprises an excitatory/inhibitory neuronal network that maintains a finely tuned balance of activity critical for normal functioning. Excitatory activity in the basolateral amygdala (BLA), a brain region that plays a central role in emotion and motivational processing, is tightly regulated by a relatively small population of gamma-aminobutyric acid (GABA) inhibitory neurons. Disruption in GABAergic inhibition in the BLA can occur when there is a loss of local GABAergic interneurons, alterations in GABAA receptor activation, or dysregulation of mechanisms that modulate BLA GABAergic inhibition. Disruptions in GABAergic control of the BLA emerge during development, in aging populations, or after a trauma, ultimately resulting in hyperexcitability. BLA hyperexcitability manifests behaviorally as an increase in anxiety, emotional dysregulation, or the development of seizure activity. This article reviews the anatomy, development, and physiology of the GABAergic system in the BLA, and circuits that modulate GABAergic inhibition, including the dopaminergic, serotonergic, noradrenergic, and cholinergic systems. We highlight how alterations in various neurotransmitter receptors, including the acid sensing ion channel 1a (ASIC1a), cannabinoid receptor 1 (CB1), and glutamate receptor subtypes, expressed on BLA interneurons, modulate GABAergic transmission and how defects of these systems affects inhibitory tonus within the BLA. Finally, we discuss alterations in the BLA GABAergic system in neurodevelopmental (autism/Fragile X syndrome) and neurodegenerative (Alzheimer’s disease) diseases, and after the development of epilepsy, anxiety, and traumatic brain injury. A more complete understanding of the intrinsic excitatory/inhibitory circuit balance of the amygdala and how imbalances in inhibitory control contribute to excessive BLA excitability will guide the development of novel therapeutic approaches in neuropsychiatric diseases.

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Role of presynaptic 5-HT1A and 5-HT3 receptors in modulation of synaptic GABA transmission in dissociated rat basolateral amygdala neurons

Cited by 68 publications

References 21 publications

Stress Impairs 5-HT2A Receptor-Mediated Serotonergic Facilitation of GABA Release in Juvenile Rat Basolateral Amygdala

Stress Impairs 5-HT2A Receptor-Mediated Serotonergic Facilitation of GABA Release in Juvenile Rat Basolateral Amygdala

Input-specific contributions to valence processing in the amygdala

The basolateral amygdala γ‐aminobutyric acidergic system in health and disease

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