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Sucrose-induced plasticity in the basolateral amygdala in a 'comfort' feeding paradigm.

ABSTRACT: A history of intermittent, limited sucrose intake (LSI) attenuates the hypothalamic-pituitary-adrenocortical (HPA) axis stress response, and neuronal activity in the basolateral amygdala (BLA) is necessary for this HPA-dampening. LSI increases the expression of plasticity-associated genes in the BLA; however, the nature of this plasticity is unknown. As BLA principal neuron activity normally promotes HPA responses, the present study tests the hypothesis that LSI decreases stress-excitatory BLA output by decreasing glutamatergic and/or increasing GABAergic inputs to BLA principal neurons. Male rats with unlimited access to chow and water were given additional access to 4 ml of sucrose (30%) or water twice daily for 14 days, and BLA structural and functional plasticity was assessed by quantitative dual immunolabeling and whole-cell recordings in brain slices. LSI increased vesicular glutamate transporter 1-positive (glutamatergic) appositions onto parvalbumin-positive inhibitory interneurons, and this was accompanied by increased expression of pCREB, a marker of neuronal activation that is mechanistically linked with plasticity, within parvalbumin interneurons. LSI also increased the paired-pulse facilitation of excitatory, but not inhibitory synaptic inputs to BLA principal neurons, without affecting postsynaptic excitatory or miniature excitatory and inhibitory postsynaptic currents, suggesting a targeted decrease in the probability of evoked synaptic excitation onto these neurons. Collectively, these results suggest that LSI decreases BLA principal neuron output by increasing the excitatory drive to parvalbumin inhibitory interneurons, and decreasing the probability of evoked presynaptic glutamate release onto principal neurons. Our data further imply that palatable food consumption blunts HPA stress responses by decreasing the excitation-inhibition balance and attenuating BLA output.

SUBMITTER: Packard AEB

PROVIDER: S-EPMC5688001 | biostudies-literature | 2017 Dec

REPOSITORIES: biostudies-literature

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Sucrose-induced plasticity in the basolateral amygdala in a 'comfort' feeding paradigm.

Packard Amy E B AEB Di Shi S Egan Ann E AE Fourman Sarah M SM Tasker Jeffrey G JG Ulrich-Lai Yvonne M YM

Brain structure & function 20170608 9

A history of intermittent, limited sucrose intake (LSI) attenuates the hypothalamic-pituitary-adrenocortical (HPA) axis stress response, and neuronal activity in the basolateral amygdala (BLA) is necessary for this HPA-dampening. LSI increases the expression of plasticity-associated genes in the BLA; however, the nature of this plasticity is unknown. As BLA principal neuron activity normally promotes HPA responses, the present study tests the hypothesis that LSI decreases stress-excitatory BLA o ...[more]

PMID: 28597100

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Project description:The basolateral amygdala (BLA) integrates sensory input from cortical and subcortical regions, a function that requires marked synaptic plasticity. Here we provide evidence that cytochrome P450 aromatase (AROM), the enzyme converting testosterone to 17?-estradiol (E2), contributes to the regulation of this plasticity in a sex-specific manner. We show that AROM is expressed in the BLA, particularly in the basolateral nucleus (BL), in male and female rodents. Systemic administration of the AROM inhibitor letrozole reduced spine synapse density in the BL of adult female mice but not in the BL of male mice. Similarly, in organotypic corticoamygdalar slice cultures from immature rats, treatment with letrozole significantly reduced spine synapses in the BL only in cultures derived from females. In addition, letrozole sex-specifically altered synaptic properties in the BL: in acute slices from juvenile (prepubertal) female rats, wash-in of letrozole virtually abolished long-term potentiation (LTP), whereas it did not prevent the generation of LTP in the slices from males. Together, these data indicate that neuron-derived E2 modulates synaptic plasticity in rodent BLA sex-dependently. As protein expression levels of AROM, estrogen and androgen receptors did not differ between males and females and were not sex-specifically altered by letrozole, the findings suggest sex-specific mechanisms of E2 signaling.SIGNIFICANCE STATEMENT The basolateral amygdala (BLA) is a key structure of the fear circuit. This research reveals a sexually dimorphic regulation of synaptic plasticity in the BLA involving neuronal aromatase, which produces the neurosteroid 17?-estradiol (E2). As male and female neurons in rodent BLA responded differently to aromatase inhibition both in vivo and in vitro, our findings suggest that E2 signaling in BLA neurons is regulated sex-dependently, presumably via mechanisms that have been established during sexual determination. These findings could be relevant for the understanding of sex differences in mood disorders and of the side effects of cytochrome P450 aromatase inhibitors, which are frequently used for breast cancer therapy.

Project description:To study the molecular mediators of naturally rewarding effects of palatable food we used a model of palatable âsnackingâ (Ulrich-Lai et al., 2007) in which rats are given chronic, brief access to a limited amount of sucrose solution (30%). Single housed, male Long-Evans rats (250g) (n=12 per group) from Harlan Labs (Indianapolis, IN) received normal rat chow (Harlan Teklad) and water ad libitum for the duration of the experiment. After a one-week period of acclimation, rats were randomly assigned to drink treatment groups of either 30% sucrose solution or water. Rats received a 14-day regimen of twice daily (9:30 and 15:30) brief (maximum of 30 minutes) limited (up to 4 mL) access of their assigned drink solution. Drink solutions were delivered via a graduated sipper placed onto the cage top in addition to the existing water bottle and sippers were immediately removed when the animal had consumed 4mL or after the 30-minute access period, whichever occurred first. Drink intake, food intake, and body weight were monitored throughout the experiment to verify that the rats learned to drink sucrose, that they adjusted chow intake for calories consumed from sucrose (~10%), and that there was no effect on body weight gain as is normally seen with this model (Ulrich-Lai et al., 2007). Drink treatment terminated on day 14 and at 8:00 on the morning of day 15, the rats were sacrificed by rapid decapitation. BLA tissue was dissected, RNA extracted, and gene expression changes between water and sucrose groups were accessed by microarray. We used microarray to assess the changes in gene expression in the BLA of rats that have had a history of sucrose snacks (n=12) vs control (n=12). Rats received access (up to 4 mL) to extra bottles containing water (control) or 30% sucrose twice daily for 14 days. Rats had ab lib access to chow and water for the duration of the experiment. Rats were sacrificed the morning of day 15 and the BLA was removed for microarray analysis. Functional cluster analysis was performed on the list of 145 significantly upregulated genes using Ingenuity Pathway Analysis (Ingenuity Systems, Redwood City, CA). See supplementary file at the foot of this record.

Dataset Information

Sucrose-induced plasticity in the basolateral amygdala in a 'comfort' feeding paradigm.

Publications

Sucrose-induced plasticity in the basolateral amygdala in a 'comfort' feeding paradigm.

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