Consciousness in Jawless Fishes

Abstract

Jawless fishes were the first vertebrates to evolve. It is thus important to investigate them to determine whether consciousness was acquired in the common ancestor of all vertebrates. Most jawless fish lineages are extinct, and cyclostomes (lampreys and hagfish) are the sole survivors. Here, I review the empirical knowledge on the neurobiology of cyclostomes with special reference to recently proposed "markers" of primary, minimal consciousness. The adult lamprey appears to meet the neuroanatomical criteria but there is a practical limitation to behavioral examination of its learning ability. In addition, the consciousness-related neuroarchitecture of larvae and its reconstruction during metamorphosis remain largely uninvestigated. Even less is known of hagfish neurobiology. The hagfish forebrain forms the central prosencephalic complex, and the homology of its components to the brain regions of other vertebrates needs to be confirmed using modern techniques. Nevertheless, as behavioral responses to olfactory stimuli in aquariums have been reported, it is easier to investigate the learning ability of the hagfish than that of the lamprey. Based on these facts, I finally discuss the potential future directions of empirical studies for examining the existence of consciousness in jawless fishes.

Keywords: ammocoetes; cyclostome; hagfish; lamprey; minimal consciousness; primary consciousness.

FIGURE 1

Phylogenetic tree of early vertebrates and brain sections of the cyclostomes. (A) Cladogram showing the postulated relationships of the jawless fishes and the Gnathostomata (jawed fishes) based on morphological characters (based on Benton, 2015). (B–E) Lateral view of adult lamprey (Lethenteron camtschaticum, B), dorsal view of the brain (C), and its transverse brain sections at the forebrain (D) and midbrain (E) levels. The laminated structure of the optic tectum is magnified in the inset of (E). (F–I) Lateral view of larval lamprey (F), dorsal view of the brain (G), and its transverse brain sections at the forebrain (H) and midbrain (I) levels. The photograph for (G) is reproduced from Suzuki and Grillner (2018). (J–M) Lateral view of adult hagfish (Eptatretus burgeri, J), dorsal view of the brain (K), and its transverse brain sections at the forebrain (L) and midbrain (M) levels. Sections are immunostained by anti-acetylated tubulin antibody (Sigma, T6793, magenta) and counterstained with Fluorescent Nissl Stain (Invitrogen N21480, green). acoctl, area octavolateralis; cpc, central prosencephalic complex; dmtn, dorsomedial telencephalic nucleus; hab, habenular ganglion; lp, lateral pallium; mp, medial pallium; nupo, nuclei praeoptici; pal, pallium; po, pineal organ; tect, tectum; rdV, radix descendens nervi trigemini; rs, formation reticularis, pars superior; vl, ventriculus lateralis; Vmm, nucleus motorius magnocellularis nervi trigemini; vq ventriculus quartus. Scale bars: 1 mm for (C,G,K); 500 μm for (D,E,L,M); 200 μm for (H,I).