Coupling of activity, metabolism and behaviour across the Drosophila brain

Mann, Kevin; Deny, Stéphane; Ganguli, Surya; Clandinin, Thomas R.

doi:10.1038/s41586-021-03497-0

Cited by 62 publications

(40 citation statements)

References 40 publications

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“…Similar to the conceptual shift from regional and cellular perspectives towards distributed brain networks and neuronal ensembles 60,61 , our discovery advances the notion that mitochondria may regulate brain function and behavior through distributed mito-networks. This notion is consistent with recent evidence of metabolic coupling among distributed patterns of behavior-related neural activity in Drosophila 12 .…”

supporting

confidence: 92%

“…While we cannot directly explain the apparent harmonization of mitochondrial function across brain regions, it may arise from three main factors. First, mitochondria could respond to differences in neuronal circuit functioning, in agreement with observed coupling of neuronal and metabolic activities 12 , such that the cellular infrastructure of neural circuits that fire together not only wire together, but also generate similar mitochondria. A second possibility is that brain regions which are regularly co-activated, i.e., within the same functional networks, harbor similar levels of receptors for neuroendocrine factors (stress and sex steroids) known to influence 1 6 mitochondrial biogenesis and/or functional specialization 62,63 .…”

supporting

confidence: 61%

“…Further, we showed that bioenergetic connectivity was tightly linked with gene co-expression and structural connectivity, thereby providing converging evidence of mitochondria-based networks across modalities. This study synergizes with recent work in Drosophila 12 , providing the technical and empirical foundation to bring mitochondrial biology into brain-wide, network-based models of neural systems in mammals 19,20 . Applied to mitochondria, network-based analytics will contribute to develop more accurate maps, and eventually an understanding of what determines mitochondrial and metabolic properties across interacting neural circuits.…”

mentioning

confidence: 58%

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Brain mitochondrial diversity and network organization predict anxiety-like behavior in mice

Rosenberg

Saggar

Rogu

et al. 2021

Preprint

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The brain and behavior are under energetic constraints, which are likely driven by mitochondrial energy production capacity. However, the mitochondria-behavior relationship has not been systematically studied on a brain-wide scale. Here we examine the association between mitochondrial health index and stress-related behaviors in mice with diverse mitochondrial and behavioral phenotypes. Miniaturized assays of mitochondrial respiratory chain function and mitochondrial DNA (mtDNA) content were deployed on 571 samples from 17 brain regions. We find specific patterns of mito-behavior associations that vary across brain regions and behaviors. Furthermore, multi-slice network analysis applied to our brain-wide mitochondrial dataset identified three large-scale networks of brain regions. A major network composed of cortico-striatal regions exhibits highest mitochondria-behavior correlations, suggesting that this mito-based network is functionally significant. Mito-based networks can also be recapitulated using correlated gene expression and structural connectome data, thereby providing convergent multimodal evidence of mitochondrial functional organization anchored in gene, brain and behavior.

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supporting

confidence: 92%

supporting

confidence: 61%

mentioning

confidence: 58%

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Brain mitochondrial diversity and network organization predict anxiety-like behavior in mice

Rosenberg

Saggar

Rogu

et al. 2021

Preprint

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“…We could have also considered more complex non-linear relationships between metabolic costs and neural activity. However, the main conclusions of our work are not affected by the exact specification of the cost function, and it has been demonstrated that the linear relationship is a reasonable assumption (59). We also note that we have not included costs associated to downstream precision 1/σ late .…”

Section: Descriptive Behavioral Modelsmentioning

confidence: 75%

“…1) can be directly related to the amount of neural activity and its associated variability (13) (methods, Figures S2 and S3). Moreover, it has been recently shown that the relationship between neural activity and energy expenditure in the brain is nearly linear (59).…”

Section: Efficient Perception and Rational Inattentionmentioning

confidence: 99%

Rational inattention in mice

Grujic

Brus

Burdakov

et al. 2021

Preprint

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Behavior exhibited by humans and other organisms is generally inconsistent and biased, and thus is often labeled irrational. However, the origins of this seemingly suboptimal behavior remain elusive. We developed a behavioral task and normative framework to reveal how organisms should allocate their limited processing resources such that there is an advantage to being imprecise and biased for a given metabolic investment that guarantees maximal utility. We found that mice act as rational-inattentive agents by adaptively allocating their sensory resources in a way that maximizes reward consumption in novel stimulus-reward association environments. Surprisingly, perception to commonly occurring stimuli was relatively imprecise, however this apparent statistical fallacy implies "awareness" and efficient adaptation to their neurocognitive limitations. Interestingly, distributional reinforcement learning mechanisms efficiently regulate sensory precision via top-down normalization. These findings establish a neurobehavioral foundation for how organisms efficiently perceive and adapt to environmental states of the world within the constraints imposed by neurobiology.

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Spatial Regulation Control of Oxygen Metabolic Consumption in Mouse Brain

Zhou

2022

Advanced Science

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The mammalian brain relies on significant oxygen metabolic consumption to fulfill energy supply, brain function, and neural activity. In this study, in vivo electrochemistry is combined with physiological and ethological analyses to explore oxygen metabolic consumption in an area of the mouse brain that includes parts of the primary somatosensory cortex, primary motor cortex, hippocampus, and striatum. The oxygen levels at different locations of this boundary section are spatially resolved by measuring the electrical current in vivo using ingeniously designed anti‐biofouling carbon fiber microelectrodes. The characteristics of the current signals are further interpreted by simultaneously recording the physiological responses of the mice. Additionally, ethological tests are performed to validate the correlation between oxygen levels and mouse behavior. It is found that high‐dose caffeine injection can evoke spatial variability in oxygen metabolic consumption between the four neighboring brain regions. It is proposed that the oxygen metabolic consumption in different brain regions is not independent of each other but is subject to spatial regulation control following the rules of “rank of brain region” and “relative distance.” Furthermore, as revealed by in vivo wireless electrochemistry and ethological analysis, mice are at risk of neuronal damage from long‐term intake of high‐dose caffeine.

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Coupling of activity, metabolism and behaviour across the Drosophila brain

Cited by 62 publications

References 40 publications

Brain mitochondrial diversity and network organization predict anxiety-like behavior in mice

Brain mitochondrial diversity and network organization predict anxiety-like behavior in mice

Rational inattention in mice

Spatial Regulation Control of Oxygen Metabolic Consumption in Mouse Brain

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