SEARCHNARRATIVE_REVIEWneurology, biomedical research

narrative_review·neurology, biomedical research, preclinical research·PMC10579582

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

Frontiers in Physiology · 7 authors, 5 centres

AI SUMMARY

FIDELITY 100%

This summary was generated by AI from a single paper. It has not been reviewed by a clinician and is not clinical advice. Verify against the source before acting on it.

AGENT 01 · STRUCTURED SUMMARY

TRACE TO SOURCE

“

TL;DR

This narrative review compares the nervous system organization of the soft-bodied sea slug Pleurobranchaea with vertebrates, arguing that a common modular blueprint for decision and action selection may have evolved in a soft-bodied bilaterian ancestor.

Full summary

881 CHARS

This narrative review synthesizes comparative neuroscience data to propose that the modular neural organization for decision-making and action selection observed in complex vertebrates may have originated in simpler, soft-bodied invertebrates. The authors compare the nervous system of the gastropod Pleurobranchaea with vertebrate and insect systems, highlighting functional analogies in specific neural modules: the gastropod feeding network is analogous to vertebrate basal ganglia and hypothalamus for action selection and motivation; the A-cluster neurons are analogous to the vertebrate reticular system for premotor function; and the pedal ganglia are analogous to the spinal cord for motor pattern generation. The review introduces the subepithelial network (SeN) as a potential simple analog of vertebrate pallial derivatives for computing incentive and stimulus location.

STUDY TYPE

narrative_review

SPECIALTY

neurology

SUMMARISED BY

AI pipeline

FIDELITY CHECK

100% · A

ORIGINAL PAPER

PMC10579582

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

Frontiers in Physiology

READ THE FULL PAPER

ABSTRACT

Abstract 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. Keywords: evolution, homology, analogy, pallium, reticular system, Pleurobranchaea

CITATION EXPORT

Ekaterina D Gribkova, Colin A Lee, Jeffrey W Brown et al.. A common modular design of nervous systems originating in soft-bodied invertebrates. Frontiers in Physiology. (2023). https://doi.org/10.3389/fphys.2023.1263453

AUTHORS

7 · 5 CENTRES

Ekaterina D Gribkova, Colin A Lee, Jeffrey W Brown, Jilai Cui, Yichen Liu, Tigran Norekian, Rhanor Gillette

1 Coordinated Science Laboratory, University of Illinois at Urbana-Champaign, Urbana, IL, United States
2 Neuroscience Program, University of Illinois at Urbana-Champaign, Urbana, IL, United States
3 Stanson Toshok Center for Brain Function and Repair, Rosalind Franklin University of Medicine and Science, North Chicago, IL, United States
4 Department of Molecular & Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL, United States
5 Whitney Laboratory for Marine Biosciences, University of Florida, St. Augustine, FL, United States