Neuronal Segmentation in Cephalopod Arms

Overview

Journal bioRxiv

Date 2024 Jun 10

PMID 38853825

Authors

Cassady S Olson

Natalie Grace Schulz

Clifton W Ragsdale

Affiliations

Soon will be listed here.

Abstract

The prehensile arms of the cephalopod are among these animals most remarkable features, but the neural circuitry governing arm and sucker movements remains largely unknown. We studied the neuronal organization of the adult axial nerve cord (ANC) of with molecular and cellular methods. The ANCs, which lie in the center of every arm, are the largest neuronal structures in the octopus, containing four times as many neurons as found in the central brain. In transverse cross section, the cell body layer (CBL) of the ANC wraps around its neuropil (NP) with little apparent segregation of sensory and motor neurons or nerve exits. Strikingly, when studied in longitudinal sections, the ANC is segmented. ANC neuronal cell bodies form columns separated by septa, with 15 segments overlying each pair of suckers. The segments underlie a modular organization to the ANC neuropil: neuronal cell bodies within each segment send the bulk of their processes directly into the adjoining neuropil, with some reaching the contralateral side. In addition, some nerve processes branch upon entering the NP, forming short-range projections to neighboring segments and mid-range projections to the ANC segments of adjoining suckers. The septa between the segments are employed as ANC nerve exits and as channels for ANC vasculature. Cellular analysis establishes that adjoining septa issue nerves with distinct fiber trajectories, which across two segments (or three septa) fully innervate the arm musculature. Sucker nerves also use the septa, setting up a nerve fiber "suckerotopy" in the sucker-side of the ANC. Comparative anatomy suggests a strong link between segmentation and flexible sucker-laden arms. In the squid , the arms and the sucker-rich club of the tentacles have segments, but the sucker-poor stalk of the tentacles does not. The neural modules described here provide a new template for understanding the motor control of octopus soft tissues. In addition, this finding represents the first demonstration of nervous system segmentation in a mollusc.

References

Kier W . The Musculature of Coleoid Cephalopod Arms and Tentacles. Front Cell Dev Biol. 2016; 4:10. PMC: 4757648. DOI: 10.3389/fcell.2016.00010. View

Rowell C . Activity of interneurones in the arm of Octopus in response to tactile stimulation. J Exp Biol. 1966; 44(3):589-605. DOI: 10.1242/jeb.44.3.589. View

Albertin C, Medina-Ruiz S, Mitros T, Schmidbaur H, Sanchez G, Wang Z . Genome and transcriptome mechanisms driving cephalopod evolution. Nat Commun. 2022; 13(1):2427. PMC: 9068888. DOI: 10.1038/s41467-022-29748-w. View

Rossi F, GRAZIADEI P . [New data on the nervous system of the tentacles of cephalopds. IV. Innervation of the suckers of Octopus vulgaris]. Acta Anat Suppl (Basel). 1958; 34(32):1-79. View

Kier W . The musculature of squid arms and tentacles: Ultrastructural evidence for functional differences. J Morphol. 2018; 185(2):223-239. DOI: 10.1002/jmor.1051850208. View

Grant P, Pant H . Compartment-Specific Phosphorylation of Squid Neurofilaments. Methods Enzymol. 2016; 568:615-33. DOI: 10.1016/bs.mie.2015.09.033. View

Arshadi C, Gunther U, Eddison M, Harrington K, Ferreira T . SNT: a unifying toolbox for quantification of neuronal anatomy. Nat Methods. 2021; 18(4):374-377. DOI: 10.1038/s41592-021-01105-7. View

Gutfreund Y, Flash T, Yarom Y, Fiorito G, Segev I, Hochner B . Organization of octopus arm movements: a model system for studying the control of flexible arms. J Neurosci. 1996; 16(22):7297-307. PMC: 6578955. View

Saga Y, Takeda H . The making of the somite: molecular events in vertebrate segmentation. Nat Rev Genet. 2001; 2(11):835-45. DOI: 10.1038/35098552. View

10.

Wagele J, Letsch H, Klussmann-Kolb A, Mayer C, Misof B, Wagele H . Phylogenetic support values are not necessarily informative: the case of the Serialia hypothesis (a mollusk phylogeny). Front Zool. 2009; 6:12. PMC: 2710323. DOI: 10.1186/1742-9994-6-12. View

11.

Laschi C, Mazzolai B, Cianchetti M . Soft robotics: Technologies and systems pushing the boundaries of robot abilities. Sci Robot. 2020; 1(1). DOI: 10.1126/scirobotics.aah3690. View

12.

Piperno G, Fuller M . Monoclonal antibodies specific for an acetylated form of alpha-tubulin recognize the antigen in cilia and flagella from a variety of organisms. J Cell Biol. 1985; 101(6):2085-94. PMC: 2114011. DOI: 10.1083/jcb.101.6.2085. View

13.

Rus D, Tolley M . Design, fabrication and control of soft robots. Nature. 2015; 521(7553):467-75. DOI: 10.1038/nature14543. View

14.

Baratte S, Bonnaud L . Evidence of early nervous differentiation and early catecholaminergic sensory system during Sepia officinalis embryogenesis. J Comp Neurol. 2009; 517(4):539-49. DOI: 10.1002/cne.22174. View

15.

Wanninger A, Wollesen T . The evolution of molluscs. Biol Rev Camb Philos Soc. 2018; 94(1):102-115. PMC: 6378612. DOI: 10.1111/brv.12439. View

16.

GRAZIADEI P . Sensory receptor cells and related neurons in cephalopods. Cold Spring Harb Symp Quant Biol. 1965; 30:45-57. DOI: 10.1101/sqb.1965.030.01.008. View

17.

Hou B, Zhang D, Zhao S, Wei M, Yang Z, Wang S . Scalable and DiI-compatible optical clearance of the mammalian brain. Front Neuroanat. 2015; 9:19. PMC: 4338786. DOI: 10.3389/fnana.2015.00019. View

18.

Giribet G, Okusu A, Lindgren A, Huff S, Schrodl M, Nishiguchi M . Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons. Proc Natl Acad Sci U S A. 2006; 103(20):7723-8. PMC: 1472512. DOI: 10.1073/pnas.0602578103. View

19.

Sivitilli D, Smith J, Gire D . Lessons for Robotics From the Control Architecture of the Octopus. Front Robot AI. 2022; 9:862391. PMC: 9339708. DOI: 10.3389/frobt.2022.862391. View

20.

ALTMAN J . Control of accept and reect reflexes in the octopus. Nature. 1971; 229(5281):204-6. DOI: 10.1038/229204a0. View