Internal states drive nutrient homeostasis by modulating exploration-exploitation trade-off
Abstract
Internal states can profoundly alter the behavior of animals. A quantitative understanding of the behavioral changes upon metabolic challenges is key to a mechanistic dissection of how animals maintain nutritional homeostasis. We used an automated video tracking setup to characterize how amino acid and reproductive states interact to shape exploitation and exploration decisions taken by adult Drosophila melanogaster. We find that these two states have specific effects on the decisions to stop at and leave proteinaceous food patches. Furthermore, the internal nutrient state defines the exploration-exploitation trade-off: nutrient-deprived flies focus on specific patches while satiated flies explore more globally. Finally, we show that olfaction mediates the efficient recognition of yeast as an appropriate protein source in mated females and that octopamine is specifically required to mediate homeostatic postmating responses without affecting internal nutrient sensing. Internal states therefore modulate specific aspects of exploitation and exploration to change nutrient selection.
Data availability
-
Data from: Internal states drive nutrient homeostasis by modulating exploration-exploitation trade-offAvailable at Dryad Digital Repository under a CC0 Public Domain Dedication.
Article and author information
Author details
Funding
Fundação para a Ciência e a Tecnologia (PTDC/BIA-BCM/118684/2010)
- Carlos Ribeiro
Human Frontier Science Program (RGP0022/2012)
- Aldo A Faisal
- Carlos Ribeiro
Champalimaud Foundation
- Verónica María Corrales-Carvajal
- Carlos Ribeiro
Fundação para a Ciência e a Tecnologia (Graduate Student Fellowship, SFRH/BD/51113/2010)
- Verónica María Corrales-Carvajal
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Iain D Couzin, Max Planck Institute for Ornithology, Germany
Version history
- Received: July 22, 2016
- Accepted: October 20, 2016
- Accepted Manuscript published: October 22, 2016 (version 1)
- Accepted Manuscript updated: October 24, 2016 (version 2)
- Version of Record published: November 14, 2016 (version 3)
Copyright
© 2016, Corrales-Carvajal et al.
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 4,496
- views
-
- 931
- downloads
-
- 83
- citations
Views, downloads and citations are aggregated across all versions of this paper published by eLife.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Genetics and Genomics
- Neuroscience
Genome-wide association studies have revealed >270 loci associated with schizophrenia risk, yet these genetic factors do not seem to be sufficient to fully explain the molecular determinants behind this psychiatric condition. Epigenetic marks such as post-translational histone modifications remain largely plastic during development and adulthood, allowing a dynamic impact of environmental factors, including antipsychotic medications, on access to genes and regulatory elements. However, few studies so far have profiled cell-specific genome-wide histone modifications in postmortem brain samples from schizophrenia subjects, or the effect of antipsychotic treatment on such epigenetic marks. Here, we conducted ChIP-seq analyses focusing on histone marks indicative of active enhancers (H3K27ac) and active promoters (H3K4me3), alongside RNA-seq, using frontal cortex samples from antipsychotic-free (AF) and antipsychotic-treated (AT) individuals with schizophrenia, as well as individually matched controls (n=58). Schizophrenia subjects exhibited thousands of neuronal and non-neuronal epigenetic differences at regions that included several susceptibility genetic loci, such as NRG1, DISC1, and DRD3. By analyzing the AF and AT cohorts separately, we identified schizophrenia-associated alterations in specific transcription factors, their regulatees, and epigenomic and transcriptomic features that were reversed by antipsychotic treatment; as well as those that represented a consequence of antipsychotic medication rather than a hallmark of schizophrenia in postmortem human brain samples. Notably, we also found that the effect of age on epigenomic landscapes was more pronounced in frontal cortex of AT-schizophrenics, as compared to AF-schizophrenics and controls. Together, these data provide important evidence of epigenetic alterations in the frontal cortex of individuals with schizophrenia, and remark for the first time on the impact of age and antipsychotic treatment on chromatin organization.
-
- Neuroscience
Combining information from multiple senses is essential to object recognition, core to the ability to learn concepts, make new inferences, and generalize across distinct entities. Yet how the mind combines sensory input into coherent crossmodal representations - the crossmodal binding problem - remains poorly understood. Here, we applied multi-echo fMRI across a four-day paradigm, in which participants learned 3-dimensional crossmodal representations created from well-characterized unimodal visual shape and sound features. Our novel paradigm decoupled the learned crossmodal object representations from their baseline unimodal shapes and sounds, thus allowing us to track the emergence of crossmodal object representations as they were learned by healthy adults. Critically, we found that two anterior temporal lobe structures - temporal pole and perirhinal cortex - differentiated learned from non-learned crossmodal objects, even when controlling for the unimodal features that composed those objects. These results provide evidence for integrated crossmodal object representations in the anterior temporal lobes that were different from the representations for the unimodal features. Furthermore, we found that perirhinal cortex representations were by default biased towards visual shape, but this initial visual bias was attenuated by crossmodal learning. Thus, crossmodal learning transformed perirhinal representations such that they were no longer predominantly grounded in the visual modality, which may be a mechanism by which object concepts gain their abstraction.