Vagal input to the enteric nervous system.

Background The enteric nervous system (ENS) of the gastrointestinal tract has traditionally been viewed as a system of ganglia that operates largely independently of the brain and spinal cord. Because of this postulated autonomy, the ENS has even been characterised as the “little brain” or the “second brain.” Recent neural tracing studies, however, challenge this canon of ENS autonomy. The view that the ENS is independent can be traced to several types of observation. Early research on the relationship of the ENS to the central nervous system (CNS) noted that the ENS could support motor activity and a number of local reflexes when the viscera were decentralised or isolated. Langley (1922), in his seminal analyses, reinforced the idea of a largely autonomous ENS by noting that the preganglionic axons projecting to the ENS were far outnumbered by the multitude of enteric neurones in the viscera. In the case of the vagus nerve in particular, Langley envisioned a few specialised “mother cells” or “vagal cells” in the ENS that were contacted by preganglionic inputs and that then distributed the relatively small number of inputs to a bigger group of eVector neurones within the enteric plexuses. In a related but more modern view, Wood (1987) suggested that autonomic preganglionics might project to “command neurones” within the ENS. On the sensory side, early observations also noted that individuals with intact peripheral nerves connecting the ENS and CNS had little awareness of visceral aVerent feedback. Although the view of an all-but-autonomous ENS still tends to dominate thinking and teaching about the innervation of the gastrointestinal tract, it should be stressed that the concept is based on inconclusive premises. For example, although the spinal cord separated from the brain still supports a number of reflexes, it is not typically inferred that the cord normally operates independently of the brain. Although preganglionic axons may be outnumbered by enteric neurones, it is problematic to gauge preganglionic influences or organisation without information about ramifications or divergence of the eVerents. Although much visceral aVerent traYc does not reach awareness, it does not follow that aVerent feedback is limited. Furthermore, it might be noted that the traditional extrapolations arguing for ENS autonomy tend to ignore the lessons from psychosomatic medicine. Historically, then, the ideas of ENS autonomy have been based largely on indirect and/or relatively ambiguous arguments. These conclusions have been especially durable because of an absence of more direct evidence contradicting the assumptions. It has been particularly diYcult to evaluate the autonomy idea structurally because of limitations of neuroanatomical techniques. Advances in neural tracing technologies in the past few years, however, have now made it practical to collect structural observations that directly address the extent of the interconnections between the ENS and CNS. The present talk summarises a series of recent experiments using such new tracing strategies. The results question the model of