Kanwal, Jessleen K. and Coddington, Emma and Frazer, Rachel and Limbania, Daniela and Turner, Grace and Davila, Karla J. and Givens, Michael A. and Williams, Valarie and Datta, Sandeep Robert and Wasserman, Sara (2021) Internal State: Dynamic, Interconnected Communication Loops Distributed Across Body, Brain, and Time. Integrative and Comparative Biology, 61 (3). pp. 867-886. ISSN 1540-7063. PMCID PMC8623242. doi:10.1093/icb/icab101. https://resolver.caltech.edu/CaltechAUTHORS:20210623-165526504
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Abstract
Internal state profoundly alters perception and behavior. For example, a starved fly may approach and consume foods that it would otherwise find undesirable. A socially engaged newt may remain engaged in the presence of a predator, whereas a solitary newt would otherwise attempt to escape. Yet, the definition of internal state is fluid and ill-defined. As an interdisciplinary group of scholars spanning five career stages (from undergraduate to full professor) and six academic institutions, we came together in an attempt to provide an operational definition of internal state that could be useful in understanding the behavior and the function of nervous systems, at timescales relevant to the individual. In this perspective, we propose to define internal state through an integrative framework centered on dynamic and interconnected communication loops within and between the body and the brain. This framework is informed by a synthesis of historical and contemporary paradigms used by neurobiologists, ethologists, physiologists, and endocrinologists. We view internal state as composed of both spatially distributed networks (body–brain communication loops), and temporally distributed mechanisms that weave together neural circuits, physiology, and behavior. Given the wide spatial and temporal scales at which internal state operates—and therefore the broad range of scales at which it could be defined—we choose to anchor our definition in the body. Here we focus on studies that highlight body-to-brain signaling; body represented in endocrine signaling, and brain represented in sensory signaling. This integrative framework of internal state potentially unites the disparate paradigms often used by scientists grappling with body–brain interactions. We invite others to join us as we examine approaches and question assumptions to study the underlying mechanisms and temporal dynamics of internal state.
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Alternate Title: | Internal State: body-brain communication | ||||||||||||||||||||
Additional Information: | © The Author(s) 2021. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Published: 11 June 2021. We would like to thank Gurdeep Pandher for giving us permission to use and annotate his Bhangra dance performance for the figure in Box 1. Recognition and thanks to Nkem Ndefo, for a more nuanced and holistic understanding of defensive behaviors and stress. The workshop on Spatiotemporal Dynamics of Animal Communication in conjunction with the 2020 Society for Integrative and Comparative Biology (SICB) served as an important foundation in bringing us all together for this review article. Box Figure, panel B: Adapted by permission from Nature Springer: Nature Physics. Ahamed, T., Costa, A. C., & Stephens, G. J. (2021). Capturing the continuous complexity of behaviour in Caenorhabditis elegans. Nature Physics, 17(2), 275–283. The SICB symposium was supported by the National Science Foundation [IOS #2010768]. Figures were made with Biorender.com. J.K.K. is supported by a Helen Hay Whitney Fellowship, E.C. is supported by the National Science Foundation [IOS #1351129], S.R.D. is supported by the National Institutes of Health [U24NS109520, RO11DC016222, U19NS113201, and RO1NS114020] and the Simons Collaboration on the Global Brain, and S.W. is supported by the National Science Foundation [IOS #2016188]. New data and availability of data: Labanotation of Bhangra phrase was generated in LabanWriter by Valarie Williams in support of this research. The data underlying this article are available in the article. We declare no conflicts of interest. | ||||||||||||||||||||
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Subject Keywords: | sensory processing, timescales, modules, endocrine, behavior, distributed network | ||||||||||||||||||||
Issue or Number: | 3 | ||||||||||||||||||||
PubMed Central ID: | PMC8623242 | ||||||||||||||||||||
DOI: | 10.1093/icb/icab101 | ||||||||||||||||||||
Record Number: | CaltechAUTHORS:20210623-165526504 | ||||||||||||||||||||
Persistent URL: | https://resolver.caltech.edu/CaltechAUTHORS:20210623-165526504 | ||||||||||||||||||||
Official Citation: | Jessleen K Kanwal, Emma Coddington, Rachel Frazer, Daniela Limbania, Grace Turner, Karla J Davila, Michael A Givens, Valarie Williams, Sandeep Robert Datta, Sara Wasserman, Internal State: Dynamic, Interconnected Communication Loops Distributed Across Body, Brain, and Time, Integrative and Comparative Biology, Volume 61, Issue 3, September 2021, Pages 867–886, https://doi.org/10.1093/icb/icab101 | ||||||||||||||||||||
Usage Policy: | No commercial reproduction, distribution, display or performance rights in this work are provided. | ||||||||||||||||||||
ID Code: | 109555 | ||||||||||||||||||||
Collection: | CaltechAUTHORS | ||||||||||||||||||||
Deposited By: | Tony Diaz | ||||||||||||||||||||
Deposited On: | 23 Jun 2021 17:31 | ||||||||||||||||||||
Last Modified: | 01 Dec 2021 17:24 |
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