A brain atlas of the camouflaging dwarf cuttlefish,Sepia bandensis

Abstract

The dwarf cuttlefish, Sepia bandensis, a small cephalopod that exhibits dynamic camouflage, is an emerging model organism in neuroscience. Coleoid cephalopods (cuttlefish, octopus, and squid) evolved large, complex brains capable of learning, problem-solving, and memory. We used high resolution magnetic resonance imaging (MRI), deep learning, and fluorescent histology to generate a dwarf cuttlefish brain atlas and built an interactive web tool (cuttlebase.org) to host the data. Guided by observations in other cephalopods, we identified 38 brain lobes. The dwarf cuttlefish brain is partially encased in cartilage and includes two large optic lobes (74% the total volume of the brain), chromatophore lobes whose motor neurons directly innervate the skin, and a vertical lobe that has been implicated in learning and memory. Motor neurons emerging from the chromatophore lobe modulate the color, pattern, and texture of the skin to elicit camouflage. This brain atlas provides a valuable tool for exploring the neural basis of cuttlefish behavior.

Comparative brain structure and the neural network features of cuttlefish and squid

“…The central complex (CC) is encased by the cranial cartilage whereas the two optic lobes (OPLs) are partially covered at the posterior end (Figure 1B). In gross anatomical terms this diurnal cuttlefish possesses a compact brain superficially similar to those of S. officinalis (histology and MRI (3T & 9.4T) (Tompsett, 1939, Boycott, 1961, Wild et al, 2015, Ziegler et al, 2018) and S. bandensis (histology and MRI (9.4T)) (Montague et al, 2022) and shares a similar lobe arrangement as the loliginid squids (Young, 1974, Young, 1976, Young, 1977, Young, 1979, Messenger, 1979, Chung et al, 2020), including 32 lobes (15 of which are bilateral) (Figures 1-2 & Table S1).…”

“…Idiosepius , Loligo and Sepioteuthis ) and deep sea squid (e.g. Abraliopsis , Architeuthis , Bathyteuthis , Liocranchia and Pyroteuthis ) (Boycott, 1961, Young, 1974, Chung, 2014, Chung and Marshall, 2017, Liu et al, 2017b, Liu et al, 2017a, Li et al, 2018, Liu et al, 2018, Montague et al, 2022).…”

“…Understanding the gross neuroanatomy and circuit diagrams of any nervous system is the necessary first step towards understanding how evolution has shaped both brain structures and behaviours in cephalopods (Budelmann and Young, 1987, Nixon and Young, 2003, Williamson and Chrachri, 2004, Chung and Marshall, 2014, Chung and Marshall, 2017, Liu et al, 2018, Chung et al, 2020, Chung et al, 2022). In order to describe the neuroanatomy of the cuttlefish species described here, we have used the previous publications of S. officinalis and loliginid squids as a ‘baseline’, along with the few other descriptions for some brain areas that exist for other cuttlefish species (Cajal, 1917, Boycott, 1961, Young, 1974, Young, 1976, Young, 1977, Young, 1979, Messenger, 1979, Dubas et al, 1986b, Dubas et al, 1986a, Budelmann and Young, 1987, Wild et al, 2015, Liu et al, 2017a, Gonzalez-Bellido et al, 2018, Li et al, 2018, Chung et al, 2020, Montague et al, 2022).…”

“…Notably, while some of what we know around biology, ecology and physiology has also been obtained from the Indo-Pacific species, knowledge of their neuroanatomy is either sparse (e.g. S. latimanus , S. pharaonis , Sepia bandensis and Sepiella japonica ) or absent among distinctively diurnal species such as S. apama, the flamboyant cuttlefish ( Metasepia pffeferi ) and the mourning cuttlefish ( Sepia plangon ) (Norman et al, 1999, Hanlon et al, 2007, Zylinski et al, 2011, Lee et al, 2013, Yang and Chiao, 2016, Liu et al, 2017a, Li et al, 2018, Schnell et al, 2019, Mezrai et al, 2020, Lu and Chung, 2017, Montague et al, 2022).…”

“…We also chose a comparative approach, both between cuttlefish species and with squid, and investigated 2 species of decapodiform cephalopods that represent phylogenetically distinct groups and that exhibit different life modes, including the reef squid Sepioteuthis lessoniana and the diurnal reef cuttlefish, S. plangon. In addition to these species described here, another 9 cuttlefish species (Metasepia tullbergi , Sepia elegans, Sepia orbignyana, Sepia omani , S. latimanus , S. officinalis, S. pharaonis, S. bandensis, S. japonica ) were selected from published literature (Boycott, 1961, Jereb and Roper, 2005, Wild et al, 2015, Liu et al, 2017a, Li et al, 2018, Ziegler et al, 2018, Montague et al, 2022) and included for further analyses where comparative data exists. Observations on the relative enlargement of brain lobes, and brain folding are included in an extended comparison of species, relative to ecology and lifestyle as well as phylogenies mostly based on existing morphological and molecular data.…”