Evolution of cephalopod nervous systems

Abstract

Giant brains have independently evolved twice on this planet, in vertebrates and in cephalopods (Figure 1A). Thus, the brains and nervous systems of cephalopods provide an important counterpoint to vertebrates in the search for generalities of brain organization and function. Their mere existence disproves various hypotheses proposed to explain the evolution of the mind and the human brain, such as cognition and large brains evolved only in long-lived animals with complex social systems and parental care, none of which is true of cephalopods. Therefore, it is worthwhile to review what is known about the evolution of cephalopod nervous systems to consider how it informs our understanding of general principles of brain evolution.

Figure 1.. Cephalopod evolution.

(A) Evolutionary relationships of select animal clades reflecting estimated age. Schematics from phylopic.org, used with Creative Commons licenses. Chiton image used with permission by Noah Schlottman, adapted from a photo by Casey Dunn (CC BY-SA 3.0). (B) Extant cephalopod lineages, relationships based on Anderson and Lindgren, Mol. Phylogenet. Evol. (2021).

Figure 2.. Molluscan neuroanatomy.

(A) Schematic anterior view of coleoid anatomy highlighting the nervous system. Ventral is to the left and dorsal to the right. The central brain sits between the eyes and is divided into supraesophageal (red) and subesophageal (purple) masses, and is flanked by the optic lobes (green). The axial nerve cords (ANC, blue) run down the center of each of the sucker-lined arms. The mantle contains visceral organs including two gills, each connected to a branchial heart, a central systemic heart, the hepatopancreas (HP), and posterior salivary glands (PSG). (B) Schematic of an off-axis sagittal section through the central brain of Octopus bimaculoides, illustrating the distribution of lobes in the supraesophageal (red) and subesophageal (blue) masses. The subesophageal mass is divided into anterior, medial, and posterior subesophageal masses (ASM, MSM, PSM, respectively), while the supraesophageal mass contains the vertical lobe (VL), anterior and dorsal basal lobes (aBL, dBL), the frontal lobes (FL), and the buccal lobe (BL). (C) Schematic of generalized gastropod nervous system, where ganglia are connected to each other via commissures and connectives (grey). Illustrated here are the cerebral ganglion (CG, red), pleural ganglion (PlG, purple), pedal ganglion (PeG, blue), buccal ganglion (B, orange), and visceral ganglion (V, royal blue). (D) Schematic of generalized polyplacophoran nervous system, with cerebral cord (CC), lateral cord (LatC), and ventral cord (VC).

Figure 3.. Schematic of cephalopod brains demonstrates common ground plan and elaborations in coleoids.

Dorsal views of Nautilus brain (top), octopus brain (middle), and Sepia brain (bottom). (Top) In Nautilus, the supraesophageal cerebral cord (CC) and subesophageal palliovisceral cord (PVC) and pedal cord (PC) are flanked by two optic lobes (OL). The buccal ganglia (BuG) are situated outside of the central brain. (Based on Young (1965) and Ponder et al. (2019).) (Middle) The octopus brain has elaborations in the supraesophageal brain, colored in shades of red, including the vertical lobe (VL), above the buccal lobe (BuL), which is merged into the central brain below the anterior subesophageal mass (ASM). The posterior subesophageal mass (PSM) is at the top of the image. Based on O. bimaculoides. (Bottom) Similar to the octopus brain, the Sepia brain has large optic lobes and a large vertical lobe. In these animals, the buccal ganglion sits outside of the central brain, closer to the buccal mass. (Based on 3D rendering of Sepia bandensis on cuttlebase.org.)

Figure 4.. Neurogenesis is widespread in cephalopod embryos.

Neurogenic territories (marked in blue) in coleoid (octopus), molluscan trochophore, Drosophila, and zebrafish (Danio rerio) embryos. a, arm; AO, apical organ; BR, brain; CC, cerebral cord; OC, optic cord; PVC, palliovisceral cord; PC, pedal cord; SC, spinal cord; VNC, ventral nerve cord.