The Brain Structure and the Neural Network Features of the Diurnal Cuttlefish

Overview

Journal iScience

Publisher Cell Press

Date 2023 Jan 10

PMID 36624840

Authors

Wen-Sung Chung

Alejandra Lopez-Galan

Nyoman D Kurniawan

N Justin Marshall

Affiliations

Soon will be listed here.

Abstract

Cuttlefish are known for their rapid changes of appearance enabling camouflage and con-specific communication for mating or agonistic display. However, interpretation of their sophisticated behaviors and responsible brain areas is based on the better-studied squid brain atlas. Here we present the first detailed description of the neuroanatomical features of a tropical and diurnal cuttlefish, , coupled with observations on ontogenetic changes in its visual and learning centers using a suite of MRI-based techniques and histology. We then make comparisons to a loliginid squid, treating it as a 'baseline', and also to other cuttlefish species to help construct a connectivity map of the cuttlefish brain. Differences in brain anatomy and the previously unknown neural connections associated with camouflage, motor control and chemosensory function are described. These findings link brain heterogeneity to ecological niches and lifestyle, feeding hypotheses and evolutionary history, and provide a timely, new technology update to older literature.

Citing Articles

Switching by cuttlefish of preying tactics targeted at moving prey.

Jiun-Shian Wu J, Chiao C iScience. 2023; 26(11):108122.

PMID: 37876802 PMC: 10590972. DOI: 10.1016/j.isci.2023.108122.

'Arm brains' (axial nerves) of Jurassic coleoids and the evolution of coleoid neuroanatomy.

Klug C, Hoffmann R, Tischlinger H, Fuchs D, Pohle A, Rowe A Swiss J Palaeontol. 2023; 142(1):22.

PMID: 37780806 PMC: 10533608. DOI: 10.1186/s13358-023-00285-3.

Transcriptome-wide selection and validation of a solid set of reference genes for gene expression studies in the cephalopod mollusk .

Imperadore P, Cagnin S, Allegretti V, Millino C, Raffini F, Fiorito G Front Mol Neurosci. 2023; 16:1091305.

PMID: 37266373 PMC: 10230085. DOI: 10.3389/fnmol.2023.1091305.

References

Gonzalez-Bellido P, Scaros A, Hanlon R, Wardill T . Neural Control of Dynamic 3-Dimensional Skin Papillae for Cuttlefish Camouflage. iScience. 2018; 2:101. PMC: 6136899. DOI: 10.1016/j.isci.2018.03.021. View

Graindorge N, Alves C, Darmaillacq A, Chichery R, Dickel L, Bellanger C . Effects of dorsal and ventral vertical lobe electrolytic lesions on spatial learning and locomotor activity in Sepia officinalis. Behav Neurosci. 2006; 120(5):1151-8. DOI: 10.1037/0735-7044.120.5.1151. View

Darmaillacq A, Chichery R, Dickel L . Food imprinting, new evidence from the cuttlefish Sepia officinalis. Biol Lett. 2006; 2(3):345-7. PMC: 1686186. DOI: 10.1098/rsbl.2006.0477. View

Chichery R, Chanelet J . Motor responses obtained by stimulation of the peduncle lobe of Sepia officinalis in chronic experiments. Brain Res. 1978; 150(1):188-93. DOI: 10.1016/0006-8993(78)90664-9. View

Sherrard K . Cuttlebone morphology limits habitat depth in eleven species of Sepia (Cephalopoda: Sepiidae). Biol Bull. 2000; 198(3):404-14. DOI: 10.2307/1542696. View

Laan A, Gutnick T, Kuba M, Laurent G . Behavioral analysis of cuttlefish traveling waves and its implications for neural control. Curr Biol. 2014; 24(15):1737-42. DOI: 10.1016/j.cub.2014.06.027. View

El Nagar A, Osorio D, Zylinski S, Sait S . Visual perception and camouflage response to 3D backgrounds and cast shadows in the European cuttlefish, Sepia officinalis. J Exp Biol. 2021; 224(11). DOI: 10.1242/jeb.238717. View

Zylinski S, Darmaillacq A, Shashar N . Visual interpolation for contour completion by the European cuttlefish (Sepia officinalis) and its use in dynamic camouflage. Proc Biol Sci. 2012; 279(1737):2386-90. PMC: 3350684. DOI: 10.1098/rspb.2012.0026. View

Ponte G, Taite M, Borrelli L, Tarallo A, Allcock A, Fiorito G . Cerebrotypes in Cephalopods: Brain Diversity and Its Correlation With Species Habits, Life History, and Physiological Adaptations. Front Neuroanat. 2021; 14:565109. PMC: 7884766. DOI: 10.3389/fnana.2020.565109. View

10.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K . MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35(6):1547-1549. PMC: 5967553. DOI: 10.1093/molbev/msy096. View

11.

Liu Y, Chung W, Yu C, Hsu S, Chan F, Liu T . Morphological changes of the optic lobe from late embryonic to adult stages in oval squids Sepioteuthis lessoniana. J Morphol. 2017; 279(1):75-85. DOI: 10.1002/jmor.20755. View

12.

Roberts R, Pop S, Prieto-Godino L . Evolution of central neural circuits: state of the art and perspectives. Nat Rev Neurosci. 2022; 23(12):725-743. DOI: 10.1038/s41583-022-00644-y. View

13.

Schnell A, Clayton N, Hanlon R, Jozet-Alves C . Episodic-like memory is preserved with age in cuttlefish. Proc Biol Sci. 2021; 288(1957):20211052. PMC: 8370807. DOI: 10.1098/rspb.2021.1052. View

14.

Kawashima Y, Nishihara H, Akasaki T, Nikaido M, Tsuchiya K, Segawa S . The complete mitochondrial genomes of deep-sea squid (Bathyteuthis abyssicola), bob-tail squid (Semirossia patagonica) and four giant cuttlefish (Sepia apama, S. latimanus, S. lycidas and S. pharaonis), and their application to the phylogenetic.... Mol Phylogenet Evol. 2013; 69(3):980-93. DOI: 10.1016/j.ympev.2013.06.007. View

15.

Feord R, Sumner M, Pusdekar S, Kalra L, Gonzalez-Bellido P, Wardill T . Cuttlefish use stereopsis to strike at prey. Sci Adv. 2020; 6(2):eaay6036. PMC: 6949036. DOI: 10.1126/sciadv.aay6036. View

16.

Archdale M, Anraku K . Feeding behavior in scyphozoa, crustacea and cephalopoda. Chem Senses. 2005; 30 Suppl 1:i303-4. DOI: 10.1093/chemse/bjh235. View

17.

Akasaki T, Nikaido M, Tsuchiya K, Segawa S, Hasegawa M, Okada N . Extensive mitochondrial gene arrangements in coleoid Cephalopoda and their phylogenetic implications. Mol Phylogenet Evol. 2006; 38(3):648-58. DOI: 10.1016/j.ympev.2005.10.018. View

18.

Chiao C, Hanlon R . Cuttlefish camouflage: visual perception of size, contrast and number of white squares on artificial checkerboard substrata initiates disruptive coloration. J Exp Biol. 2001; 204(Pt 12):2119-25. DOI: 10.1242/jeb.204.12.2119. View

19.

Williamson R, Chrachri A . Cephalopod neural networks. Neurosignals. 2004; 13(1-2):87-98. DOI: 10.1159/000076160. View

20.

Hanlon R, Chiao C, Mathger L, Barbosa A, Buresch K, Chubb C . Cephalopod dynamic camouflage: bridging the continuum between background matching and disruptive coloration. Philos Trans R Soc Lond B Biol Sci. 2008; 364(1516):429-37. PMC: 2674088. DOI: 10.1098/rstb.2008.0270. View