The chemical brain hypothesis for the origin of nervous systems

Abstract

In nervous systems, there are two modes of transmission for the propagation of activity between cells. Synaptic transmission relies on close contact at chemical or electrical synapses while volume transmission is mediated by diffusible chemical signals and does not require direct contact. It is possible to wire complex neuronal networks by both chemical and synaptic transmission. Both types of networks are ubiquitous in nervous systems, leading to the question which of the two appeared first in evolution. This paper explores a scenario where chemically organised cellular networks appeared before synapses in evolution; a possibility supported by the presence of complex peptidergic signalling in all animals except sponges. Small peptides are ideally suited to link up cells into chemical networks. They have unlimited diversity, high diffusivity and high copy numbers derived from repetitive precursors. But chemical signalling is diffusion limited and becomes inefficient in larger bodies. To overcome this, peptidergic cells may have developed projections and formed synaptically connected networks tiling body surfaces and displaying synchronised activity with pulsatile peptide release. The advent of circulatory systems and neurohemal organs further reduced the constraint imposed on chemical signalling by diffusion. This could have contributed to the explosive radiation of peptidergic signalling systems in stem bilaterians. Neurosecretory centres in extant nervous systems are still predominantly chemically wired and coexist with the synaptic brain.

Elementary nervous systems

“…This hypothesis builds on the primacy of secretory cells as advocated by Lentz and others (see above), and is put forward for the first time in an elaborate fashion by Gáspár Jékely in this issue of Transactions [ 15 ]. Here, nervous system evolution starts from a sheet of ciliated cells.…”

“…Via division of labour, some of these cells specialize in sensory perception and neuropeptide release and become sensory-secretory cells interspersed among ciliary effector cells, as depicted in figure 7 a . In this arrangement, all tissue cells would be linked up into a chemical network made up of diffusible neuropeptides [ 15 ]. Yet, signalling via diffusion of peptides becomes inefficient in larger bodies.…”

“…Concomitant with the advent of circulatory systems, these cells can start secreting neuropeptides, henceforth called hormones, into the body fluid. To this end, their secretory endings gather into a prominent plexus, which is referred to as the neurosecretory centre or neurohemal organ [ 15 ].…”

“…Others envisaged effector cells carrying out immune functions in response to environmental microbes [ 12 ]. Finally, a strong camp emphasized the secretory nature of early neurons that may have acted at a distance on effector cells via the release of neuropeptides [ 13 – 15 ].…”

Choanoflagellates and the ancestry of neurosecretory vesicles

“…However, cognitive processes demand fast and reliable mechanisms of signal transduction. While volume transmission-based signal transmission might be sufficient for unicellular and colonial organisms, it becomes insufficient for organisms that have larger, more complex bodies [ 5 ]. Hence, synaptic signal transmission might have been crucial to allow for cognitive processes in large multicellular organisms with complex body structures.…”