Cephalopod Brains: An Overview of Current Knowledge to Facilitate Comparison With Vertebrates

Abstract

Cephalopod and vertebrate neural-systems are often highlighted as a traditional example of convergent evolution. Their large brains, relative to body size, and complexity of sensory-motor systems and behavioral repertoires offer opportunities for comparative analysis. Despite various attempts, questions on how cephalopod 'brains' evolved and to what extent it is possible to identify a vertebrate-equivalence, assuming it exists, remain unanswered. Here, we summarize recent molecular, anatomical and developmental data to explore certain features in the neural organization of cephalopods and vertebrates to investigate to what extent an evolutionary convergence is likely. Furthermore, and based on whole body and brain axes as defined in early-stage embryos using the expression patterns of homeodomain-containing transcription factors and axonal tractography, we describe a critical analysis of cephalopod neural systems showing similarities to the cerebral cortex, thalamus, basal ganglia, midbrain, cerebellum, hypothalamus, brain stem, and spinal cord of vertebrates. Our overall aim is to promote and facilitate further, hypothesis-driven, studies of cephalopod neural systems evolution.

Keywords: brain; cephalopod; evolution; neural networks; octopus.

FIGURE 1

The adult Octopus vulgaris brain. (A) Schematic outline of octopus body and the relative relationships to the main components of its nervous system. (B) A longitudinal section of the supra- and sub-esophageal mass of O. vulgaris (parasagittal plane). (C) A cross section of the vertical lobe (supra-esophageal mass), showing the five distinct gyri. The esophagus lies at the center between the supraesophageal and subesophageal mass. Sections of stained with the Cajal silver method. abL, anterior basal lobe; ASM, anterior subesophageal mass; dbL, dorsal basal lobe; eso, esophagus; ifL, inferior frontal lobe; MSM, middle subesophageal mass; PSM, posterior subesophageal mass; sbL, superior buccal lobe; sfL, superior frontal lobe; spL, subpedunculate lobe; svtL, subvertical lobe; vtL, vertical lobe. Scale bars: 500 μm.

FIGURE 2

Comparison of the early stage embryonic nervous systems in three invertebrates. (A) Acoelomorph or planula-like larva (left), a gastropod veliger larva (middle), and nautiloid embryo (right), defining the comparable topography of neural patterns (modified after permission of Tokai University Press following Shigeno et al., 2010). The cerebral-, ventral- and laterally situated neural cords are shaded in red, green and blue, respectively. Due to their diffuse nature, the homology of these nerve cords remains unclear, but the putative ancestral condition is shown for comparison. (B) Schematic drawing of embryonic brain development in O. bimaculoides (inspired to information contained in Shigeno et al., 2015), showing a transition from medullary cords to a centralized brain. The foregut or mouth (fg) initially lies at the anterior, but it moves to a more ventral position at the later stage. Reference to the A–P and D–V axes are provided. ASM, anterior sub-esophageal mass; ax, arm axial cord; CeC, cerebral cord; CG, cerebral ganglion; eso, esophagus; fg, foregut or mouth; man, mantle; MSM, middle subesophageal mass; PeC, pedal cord; PSM, posterior subesophageal mass; PvC, palliovisceral cord; SUP, supraesophageal mass.

FIGURE 3

Similarities in the developmental plans of the vertebrate spinal cord and cephalopod sub-esophageal mass. (A) Comparison of the neurogenic territories along the embryonic dorso-ventral axes. The color codes indicate the candidates of comparable territories. (B) Oblique cross-dissected views of the vertebrate spinal cord and of octopus sub-esophageal mass. Red areas indicate the midline cells in the spinal cord, and possible comparable parts of the ventral position of the sub-esophageal mass. A dorso-ventral segregation pattern of input sensory (green) or output motor neurons (blue) exists in the spinal cord, while no such segregation is obvious in the octopus sub-esophageal mass (see the text for further explanation). PeC, pedal cord; PvC, palliovisceral cord; D, dorsal; V, ventral.

FIGURE 4

A brain-wide, flat-map comparison of the mouse and octopus brain. Topographical similarities are highlighted using color-coding. Note similarities with the pallium and basal ganglia, and neurosecretory centers (hypothalamus). The hypothalamus and the octopus neurosecretory systems differ superficially in adult brains with the neurovenous tissues (Young, 1970), considered neurosecretory areas in cephalopod brain, such as the para-vertical and the sub-pedunculate that are situated more laterally together with the optic lobes (omitted for simplification in this figure). The sensory inputs and motor outputs indicate functionally equivalent centers. The maps are arranged along the embryonic A–P and D–V axes (outline of mouse brain inspired by the information included in: Rubenstein et al., 1994, 1998; Puelles and Rubenstein, 2003; Swanson, 2007). Cephalopod embryonic brains are initially cord-like, and the topographic position of adult brain centers is traced back to embryological position via successive histological observation (Marquis, 1989; Shigeno et al., 2001, 2015). The main driver pathways (see text for details) are selected following Young (1971) and Plän (1987). (mouse): Cer, cerebellum; Ctx, cerebral cortex; HB, hindbrain; Hyp, hypothalamus; Sc, superior colliculus; Str, striatum; Th, thalamus; Tg, tegmentum; (cephalopod): ARM, arm nerve cord; bL, basal lobe; fvL, frontal and vertical lobe; EYE, eyes; FUN, funnel; HEAD, head; MAN, mantle; SM, subesophageal mass; sbL, superior buccal lobe; spL, sub-pedunculate lobe; VIS, visceral organs.

FIGURE 5

The evolution of cortical territories represented by a zonation in cephalopod brain evolution. (A) Phylogram of the evolution of brain complexity and emergence (still controversial) and organization of the amacrine cells into clusters. Based on the information included in Lindgren et al. (2012), and data assembled from Young (1965a, 1977a), Nixon and Young (2003). The centers are primitively zonal or band-like (Nautilus) and they are enlarged, or centralized or reduced in more ‘evolved’ species such as cuttlefish and octopus. (B) Homology of cell types and appearance of amacrine cells or their equivalent cell types (purple) in different cephalopod species. Homology of cell types in Nautilus is also controversial when compared with other taxa, but the gross similarity of topographical distribution is apparent. Large cells (green) are commonly localized in the buccal lobe area, which are often serotonergic (Wollesen et al., 2012). Toward the posterior end of the dorsal basal lobe clusters of GABAergic cells (blue) have been identified in octopus (Cornwell et al., 1993; Ponte, 2012). Outline of supra-esophageal mass and optic lobes are exemplified as a view from top; the overall shape of the brains is simplified as that of later embryonic stage. dbL, dorsal basal lobe; ifL, inferior frontal lobe; lcL, lateral cerebral lobe; lz, laminated zone of cerebral cord; opL, optic lobe; sbL, superior buccal lobe; sfL, superior frontal lobe; spL, sub-pedunculate lobe; vtL, vertical lobe.