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.
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Acknowledgements
This work was supported by National Institutes of Health Grants R01 DK091425 (YMU), K01 DK078906 (YMU), F32 DK102334 (AEBP), T32 DK059803 (AEBP, AEE), and an Albert J. Ryan Foundation Fellowship (AEE). We would like to thank Sriparna Ghosal for her excellent technical assistance.
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Packard, A.E.B., Di, S., Egan, A.E. et al. Sucrose-induced plasticity in the basolateral amygdala in a ‘comfort’ feeding paradigm. Brain Struct Funct 222, 4035–4050 (2017). https://doi.org/10.1007/s00429-017-1454-7
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DOI: https://doi.org/10.1007/s00429-017-1454-7