Phylogeny of enteric serotonergic neurons

Area of Science:

• Neuroscience
• Evolutionary Biology
• Gastroenterology

Background:

• Serotonergic neurons are key components of the enteric nervous system (ENS).
• Previous studies identified these neurons in mammals (humans, primates, rodents, rabbits).
• The evolutionary origin and distribution across vertebrates remained unclear.

Purpose of the Study:

• To investigate the presence and distribution of enteric serotonergic neurons in lower vertebrates.
• To determine if these neurons are exclusive to mammals or more widespread.
• To pinpoint the earliest appearance of these neurons in vertebrate phylogeny.

Main Methods:

• Utilized radioautography to detect axonal uptake of 3H-serotonin, a specific marker for these neurons.
• Employed control conditions including fluoxetine, Na+-free medium, and excess nonradioactive serotonin to confirm specificity.
• Examined various vertebrate species including cyclostomes, teleosts, and amphibia, alongside invertebrate controls.

Main Results:

• Specific 3H-serotonin uptake was confirmed in enteric neurons of hagfish (cyclostomes), goldfish (teleosts), and bullfrogs (amphibia).
• No specific labeling was observed in tunicates (sea squirts) or echinoderms (sea cucumbers).
• Serotonin was detected in the intestines of hagfish and goldfish, with highest concentrations in the myenteric plexus region.

Conclusions:

• Enteric serotonergic neurons are not restricted to mammals but are a general feature of the vertebrate bowel.
• These neurons likely evolved early in vertebrate evolution, potentially originating in an ancestral chordate.
• The findings provide insights into the ancient origins of gut neurobiology.