The chemical brain hypothesis for the origin of nervous systems

In nervous systems, there are two main 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 organized 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 synchronized 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. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens’.

The chemical brain hypothesis for the origin of nervous systems

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.

Profiling the peptides in two neurohemal organs, the sinus gland and lateral nervous plexus of terrestrial isopods (Crustacea), by mass spectrometry

A comparison was made of the ultrastructure of two neurohemal organs: the sinus gland and the lateral nervous plexus of the Oniscidea (Crustacea). Reverse-phase chromatography clearly showed that the two organs contain different neuropeptides. Matrix-assisted laser desorption/ionization time-of-flight mass spectrometry proved to be an efficient tool for detecting the molecules stored in a single freshly dissected neurohemal organ. All the results combined lead us to emphasize that the sinus gland of Oniscidea stores mainly crustacean hyperglycemic hormone (CHH) and vitellogenin-inhibiting hormone; these two hormones were not characterized in the lateral nervous plexus (LNP). Smaller peptides and other molecules of the CHH family might be released by the LNP in the vicinity of the Y-organ (the ecdysteroid-producing gland).

Characterization of two myotrophic neuropeptides in the FMRFamide family from the segmental ganglia of the moth Manduca sexta: candidate neurohormones and neuromodulators

We have characterized two new members of the FMRFamide family of neuropeptides from the segmental ganglia of the tobacco hornworm Manduca sexta. Levels of peptides in ganglia used for purification were enhanced by manipulating their exposure to the steroid molting hormones. Explants of ganglia were cultured in the low-level ecdysteroid environment of diapausing pupae shown previously to evoke accumulation of FMRFamide-like immunoreactivity (FLI). Sufficient material for sequencing was obtained from 180 explanted ganglia. Extracts of ganglia were fractionated using two reverse-phase liquid chromatography procedures, and the immunoreactive fractions were subjected to sequence analysis using electrospray mass spectrometry. The sequences of the two peptides were determined to be GNSFLRFamide and DPSFLRFamide. These peptides have been named MasFLRFamide II and MasFLRFamide III, respectively; the previously characterized M. sexta FLRFamide (pEDVVHSFLRFamide) has been renamed MasFLRFamide I. The three peptides show distinctive tissue and developmental distributions as determined from fractionated extracts of larval and adult central nervous system structures and neurohemal organs. In the retrocerebral corpora cardiaca/corpora allata, MasFLRFamide I was the predominant form, while in the segmental ganglia MasFLRFamides II and III predominated. Higher levels of MasFLRFamide I and II were found in the adult, whereas there was little apparent change in the level of MasFLRFamide III upon metamorphosis. Determinations of peptide levels in fractionated hemolymph of newly emerged moths revealed that levels of MasFLRFamide I and III could exceed 10 nmol l-1. The actions of the three peptides were tested on the moth ileum. MasFLRFamides II and III were found to be stimulatory. At 1 nmol l-1, these peptides induced robust increases in the rate of rhythmic longitudinal and peristaltic waves of contractions. In contrast, MasFLRFamide I was ineffective even at 20 nmol l-1. Thus, while all three peptides have the characteristics of neurohormones in M. sexta, the physiological findings show that the heptapeptide FLRFamides have properties distinct from those of the decapeptide.