Dataset Information

Socially responsive effects of brain oxidative metabolism on aggression.

ABSTRACT: Despite ongoing high energetic demands, brains do not always use glucose and oxygen in a ratio that produces maximal ATP through oxidative phosphorylation. In some cases glucose consumption exceeds oxygen use despite adequate oxygen availability, a phenomenon known as aerobic glycolysis. Although metabolic plasticity seems essential for normal cognition, studying its functional significance has been challenging because few experimental systems link brain metabolic patterns to distinct behavioral states. Our recent transcriptomic analysis established a correlation between aggression and decreased whole-brain oxidative phosphorylation activity in the honey bee (Apis mellifera), suggesting that brain metabolic plasticity may modulate this naturally occurring behavior. Here we demonstrate that the relationship between brain metabolism and aggression is causal, conserved over evolutionary time, cell type-specific, and modulated by the social environment. Pharmacologically treating honey bees to inhibit complexes I or V in the oxidative phosphorylation pathway resulted in increased aggression. In addition, transgenic RNAi lines and genetic manipulation to knock down gene expression in complex I in fruit fly (Drosophila melanogaster) neurons resulted in increased aggression, but knockdown in glia had no effect. Finally, honey bee colony-level social manipulations that decrease individual aggression attenuated the effects of oxidative phosphorylation inhibition on aggression, demonstrating a specific effect of the social environment on brain function. Because decreased neuronal oxidative phosphorylation is usually associated with brain disease, these findings provide a powerful context for understanding brain metabolic plasticity and naturally occurring behavioral plasticity.

SUBMITTER: Li-Byarlay H

PROVIDER: S-EPMC4151721 | biostudies-literature | 2014 Aug

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Socially responsive effects of brain oxidative metabolism on aggression.

Li-Byarlay Hongmei H Rittschof Clare C CC Massey Jonathan H JH Pittendrigh Barry R BR Robinson Gene E GE

Proceedings of the National Academy of Sciences of the United States of America 20140804 34

Despite ongoing high energetic demands, brains do not always use glucose and oxygen in a ratio that produces maximal ATP through oxidative phosphorylation. In some cases glucose consumption exceeds oxygen use despite adequate oxygen availability, a phenomenon known as aerobic glycolysis. Although metabolic plasticity seems essential for normal cognition, studying its functional significance has been challenging because few experimental systems link brain metabolic patterns to distinct behavioral ...[more]

PMID: 25092297

Similar Datasets

Project description:Mood disorders such as anxiety and depression are heterogeneous disorders with many sufferers unresponsive to current pharmacological treatments. Individual differences in temperament represent one factor that may underlie symptom heterogeneity, so understanding its biological underpinnings can help pave the way to personalized therapies and improved patient outcomes. The present study uses a rodent model of temperamental differences to examine whether individual differences in emotional behavior phenotypes correspond to altered limbic brain cellular metabolism, an indicator of neuronal activity. The model uses two selectively bred rat lines - high novelty responder rats (HRs) that show highly exploratory behavior in a novel environment, active coping style and resilience to chronic mild stress compared to low novelty responder rats (LRs), which are inhibited in novel environments, display passive coping style, and are susceptible to chronic stress. Utilizing transcriptome data from a prior study in adult HR/LR rats, we first show that a preponderance of genes differing in the HR vs. LR hippocampus and amygdala are involved in cellular metabolism. This led us to then ask if oxygen consumption was altered in isolated mitochondria of the hippocampus and amygdala of HR/LR rats; here we found increased oxygen consumption reserve capacity in LR amygdala. Our last experiment examined activity of cytochrome c oxidase (COX), an enzyme responsible for ATP production and correlate of metabolic activity, in several brain regions of HR/LR rats. We found that LRs displayed higher COX activity in the dentate gyrus, prefrontal cortex, and dorsal raphe compared to HRs, with no significant HR/LR difference in nuclei of the amygdala. Correlational analyses of COX activity across brain regions suggested divergent connectivity between the prefrontal cortex, amygdala, hippocampus, and dorsal raphe of HR vs. LR rats. Together these studies point to altered cellular metabolism in the limbic brain of LR/HR animals, which may reflect altered neural circuitry that drives their divergent behavioral profiles.

Dataset Information

Socially responsive effects of brain oxidative metabolism on aggression.

Publications

Socially responsive effects of brain oxidative metabolism on aggression.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets