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A common modular design of nervous systems originating in soft-bodied invertebrates

Nervous systems of vertebrates and invertebrates show a common modular theme in the flow of information for cost-benefit decisions. Sensory inputs are incentivized by integrating stimulus qualities with motivation and memory to affect appetitive state, a system of homeostatic drives, and labelled fo...

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Autores principales: Gribkova, Ekaterina D., Lee, Colin A., Brown, Jeffrey W., Cui, Jilai, Liu, Yichen, Norekian, Tigran, Gillette, Rhanor
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10579582/
https://www.ncbi.nlm.nih.gov/pubmed/37854468
http://dx.doi.org/10.3389/fphys.2023.1263453
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author Gribkova, Ekaterina D.
Lee, Colin A.
Brown, Jeffrey W.
Cui, Jilai
Liu, Yichen
Norekian, Tigran
Gillette, Rhanor
author_facet Gribkova, Ekaterina D.
Lee, Colin A.
Brown, Jeffrey W.
Cui, Jilai
Liu, Yichen
Norekian, Tigran
Gillette, Rhanor
author_sort Gribkova, Ekaterina D.
collection PubMed
description Nervous systems of vertebrates and invertebrates show a common modular theme in the flow of information for cost-benefit decisions. Sensory inputs are incentivized by integrating stimulus qualities with motivation and memory to affect appetitive state, a system of homeostatic drives, and labelled for directionality. Appetitive state determines action responses from a repertory of possibles and transmits the decision to a premotor system that frames the selected action in motor arousal and appropriate postural and locomotion commands. These commands are then sent to the primary motor pattern generators controlling the motorneurons, with feedback at each stage. In the vertebrates, these stages are mediated by forebrain pallial derivatives for incentive and directionality (olfactory bulb, cerebral cortex, pallial amygdala, etc.) interacting with hypothalamus (homeostasis, motivation, and reward) for action selection in the forebrain basal ganglia, the mid/hindbrain reticular formation as a premotor translator for posture, locomotion, and arousal state, and the spinal cord and cranial nuclei as primary motor pattern generators. Gastropods, like the predatory sea slug Pleurobranchaea californica, show a similar organization but with differences that suggest how complex brains evolved from an ancestral soft-bodied bilaterian along with segmentation, jointed skeletons, and complex exteroceptors. Their premotor feeding network combines functions of hypothalamus and basal ganglia for homeostasis, motivation, presumed reward, and action selection for stimulus approach or avoidance. In Pleurobranchaea, the premotor analogy to the vertebrate reticular formation is the bilateral “A-cluster” of cerebral ganglion neurons that controls posture, locomotion, and serotonergic motor arousal. The A-cluster transmits motor commands to the pedal ganglia analogs of the spinal cord, for primary patterned motor output. Apparent pallial precursors are not immediately evident in Pleurobranchaea’s central nervous system, but a notable candidate is a subepithelial nerve net in the peripheral head region that integrates chemotactile stimuli for incentive and directionality. Evolutionary centralization of its computational functions may have led to the olfaction-derived pallial forebrain in the ancestor’s vertebrate descendants and their analogs in arthropods and annelids.
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spelling pubmed-105795822023-10-18 A common modular design of nervous systems originating in soft-bodied invertebrates Gribkova, Ekaterina D. Lee, Colin A. Brown, Jeffrey W. Cui, Jilai Liu, Yichen Norekian, Tigran Gillette, Rhanor Front Physiol Physiology Nervous systems of vertebrates and invertebrates show a common modular theme in the flow of information for cost-benefit decisions. Sensory inputs are incentivized by integrating stimulus qualities with motivation and memory to affect appetitive state, a system of homeostatic drives, and labelled for directionality. Appetitive state determines action responses from a repertory of possibles and transmits the decision to a premotor system that frames the selected action in motor arousal and appropriate postural and locomotion commands. These commands are then sent to the primary motor pattern generators controlling the motorneurons, with feedback at each stage. In the vertebrates, these stages are mediated by forebrain pallial derivatives for incentive and directionality (olfactory bulb, cerebral cortex, pallial amygdala, etc.) interacting with hypothalamus (homeostasis, motivation, and reward) for action selection in the forebrain basal ganglia, the mid/hindbrain reticular formation as a premotor translator for posture, locomotion, and arousal state, and the spinal cord and cranial nuclei as primary motor pattern generators. Gastropods, like the predatory sea slug Pleurobranchaea californica, show a similar organization but with differences that suggest how complex brains evolved from an ancestral soft-bodied bilaterian along with segmentation, jointed skeletons, and complex exteroceptors. Their premotor feeding network combines functions of hypothalamus and basal ganglia for homeostasis, motivation, presumed reward, and action selection for stimulus approach or avoidance. In Pleurobranchaea, the premotor analogy to the vertebrate reticular formation is the bilateral “A-cluster” of cerebral ganglion neurons that controls posture, locomotion, and serotonergic motor arousal. The A-cluster transmits motor commands to the pedal ganglia analogs of the spinal cord, for primary patterned motor output. Apparent pallial precursors are not immediately evident in Pleurobranchaea’s central nervous system, but a notable candidate is a subepithelial nerve net in the peripheral head region that integrates chemotactile stimuli for incentive and directionality. Evolutionary centralization of its computational functions may have led to the olfaction-derived pallial forebrain in the ancestor’s vertebrate descendants and their analogs in arthropods and annelids. Frontiers Media S.A. 2023-10-03 /pmc/articles/PMC10579582/ /pubmed/37854468 http://dx.doi.org/10.3389/fphys.2023.1263453 Text en Copyright © 2023 Gribkova, Lee, Brown, Cui, Liu, Norekian and Gillette. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Gribkova, Ekaterina D.
Lee, Colin A.
Brown, Jeffrey W.
Cui, Jilai
Liu, Yichen
Norekian, Tigran
Gillette, Rhanor
A common modular design of nervous systems originating in soft-bodied invertebrates
title A common modular design of nervous systems originating in soft-bodied invertebrates
title_full A common modular design of nervous systems originating in soft-bodied invertebrates
title_fullStr A common modular design of nervous systems originating in soft-bodied invertebrates
title_full_unstemmed A common modular design of nervous systems originating in soft-bodied invertebrates
title_short A common modular design of nervous systems originating in soft-bodied invertebrates
title_sort common modular design of nervous systems originating in soft-bodied invertebrates
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10579582/
https://www.ncbi.nlm.nih.gov/pubmed/37854468
http://dx.doi.org/10.3389/fphys.2023.1263453
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