The Enteric Nervous System and The Visceral Animal

Michael Gershon ( ) has referred to the Enteric Nervous System (ENS) as the "Second Brain" of vertebrates, due to it´s autonomous functioning in the abscence of central nervous system input and a the possession of a diverse and comprehensive range of endogenous neurotransmitters.

Following Romer, the ENS of extant vertebrates may be considered to be a vestige of the nerve-net that governed the behavior of the sessile chordate ancestor and it´s organization is associated with the "Visceral Animal" bauplan.

The ENS is formed from migratory neural crest cell during development and contains afferent, efferent, and sensory neurons that form two distinct types of plexus:

The ENS directly communicates with the CNS by the pharyngeal and sacral parasympathetic nerves.

Today the ENS is present in vertebrates as the myenteric plexus and the submucosal plexus - both of which are located within the mucosal wall of the gastrointestinal tract.

To summarize, the ENS,

• possesses a large array of neuroactive transmitters and peptides,
• is dedicated to trophic visceral functions,
• may operate independently of the CNS,
• and is capable of sophisticated behaviors in the absence of CNS input.

The Evolution of the Poly-Vagal Autonomic Nervous System

The autonomic nervous system of vertebrates is the central nervous system outflow that cooridinates and integrates the activity of the somatic and visceral divisions of the body in a manner that is consistent with the behavioral strategy being employed.

In moments of danger and exertion the autonomic nervous system exerts control over the baseline activity of the viscera.

While in moments of security and comfort the enteric nervous system provides hedonic modulation of emotional state and somatosensory evaluation within the central nervous system.

In this work extensive use will be made of the Polyvagal Theory of Stephen W. Porges (, , , ).

The Polyvagal Theory delineates the evolution of the vertebrate behavior as it relates to the autonomic nervous system and it´s regulation of the heart by the cranial nerves of the mid and hindbrain.

Contrary to the standard division of the autonomic nervous system into two divisions - sympathetic and parasympathetic - that innervate the viscera; we will find it more appropriate to adopt a single CNS efferent outflow division at the origin of vertebrates that will transition to a two-fold efferent outflow division at gnathostomes and a three-fold efferent outflow division within mammals.

The First Autonomic Division - The archaic Unmyelinated Parasympathetic

The somatovisceral fusion points correspond to anatomical positions in the CNS that give rise to the original vertebrate autonomic division, the archaic unmyelinated Parasympathetic Nervous System:

• The Hindbrain-Pharyngeal Complex
• The Sacral Plexus

Early in vertebrate evolution there was little coupling between the somatic and visceral bodies except at the hindbrain-pharyngeal and sacral fusion points; and no sympathetic nervous system components were present.

Agnathans are modern representatives of this condition.

The archaic vertebrates lacked the neuroanatomy required for the "somatic" central nervous system to exert coordinated control over the "visceral" tract in times of perceived danger; limiting the primary behavioral response under conditions of environmental stress to immobilization stratagies (i.e. freezing, feigning death, or catatonic state).

With the comming of mammals, a new division of the parasympathetic nervous system emerges; the myelinated parasympathetic nervous system.

This system will act to modulate the extreme expression of the older unmyelinated parasympathetic division and sympathtetic division, giving mammals the capacity for realtime environmental foraging and subtle engagement behaviors.

A Second Autonomic Division - The Sympathetic Nervous System

The sympathetic nervous system (SNS) is a real-time adaptive mobilization system facilitating fight or flight behaviors requiring global cooridination of the entire physiology of the organism.

A second HOX-cluster duplication event accompanies the emergence of the jawed vertebrates, the Gnathostomes.

With gnathostomes, we see the transformation of the first pharyngeal arch (I) into the jaws, as well as the emergence of myelin, paired fins, and the SNS.

The neural components of the first pharyngeal arch (I) are transformed into the trigeminal system.

With the emergence of jaws, paired fins, and the SNS vertebrates become capable of fight or flight behavioral strategies.

Progressive development and evolution of the SNS from the thoracolumbar regions of the spinal cord facilitates "Somatic" control over the "Viscera" under conditions of environmental challenge.

A clear progression in sympathetic nervous system innervation of the viscera can be observed as one move along the phylogenetic sequence leading from primitive gnathostomes thru tetrapods and on to mammals ( ).

As indicated by Romer, and in the light of the fusion hypothesis, SNS development may be seen an attempt by the central nervous system to exert control over the visceral nervous system under conditions of environmental challenge.

Myelination and Behavioral Response Characteristics

Myelin is formed by Oligodendrocytes in the CNS and by Schwann Cells in the PNS; both types of cell first appear in gnathostomes.

Bernard Zalc ( ) has suggested that the myelin sheath surrounding gnathostome and higher vertebrate fast conduction neurons evolved from preexisting neuronal glial cells that ensheathed conducting neurons in more primitive organisms.

Zalc suggests that these neuronal sheath cells acquired the capacity to respond to axonal signals that induced the formation of the myelin protein sheath that facilitates fast neuronal conduction.

Archaically, all cranial nerve components are assumed to be derived from the general somatic and visceral divisions and the special somatic and visceral divisions are devoted to pharyngeal functions.

Archaically, all general and special components are unmyelinated, resulting in slow response characteristics for the CNS over the ENS in times of danger.

The main danger response mechanism available to the archaic vertebrate would be via the unmyelinated parasympathetic system and the behavioral strategy is one of immobilization (i.e. freezing, feigning death...).

In gnathostomes, the emergence of sympathetic outflow requires the presence of myelin to facilitate the emergence of response times that are compatible with fight or flight behaviors.

In tetrapods the pharyngeal arches are evolutionarily modified and the muscles, cartilages, aortic arches, and nerves are co-opted for other adaptive functions, thereby introducing the special components into the cranial nerves of the more advanced vertebrates.

Remodelling of the pharyngeal arch components is accompanied by the myelinization of the pharyngeal nerves.

The Reciprocal Requirements of "Functional Welding"

Subsequent vertebrate body-plan and behavioral evolution is characterized by the emergence and/or transformation of structures that facilitate the "functional welding" of the "somatic" animal to the "visceral" animal, eventually leading to a wide diversity of sophisticated animals and ultimately to creatures like ourselves capable of abstract thought and higher-order consciousness.

The "functional welding" of the "Somatic Animal" body to the "Visceral Animal" body requires that each system is reciprocally responsive to the needs of the other and can exert influence over the action of the other in times of imperative need.

• Somatic Influence on the Viscera System - The parasympathetic, sympathetic, and neuroendocrine activity are the main mechanisms of somatic control over the viscera. The SNS and endocrine systems are especially important in coordinating global mobilization of the whole organism relative to the environment in times of challenge (i.e. Feeding, fighting, fleeing, and sex).


• Visceral Influence on the Somatic System - The Pharyngeal-Hindbrain Complex (archaic) and limbic system (amniotes) activity are the main mechanisms of visceral control over sensory processing and environmentally contingent behavior. The visceral systems provide the "hedonic value" assessments necessary for assigning cognitive "meaning" to ongoing real-time sensorimotor configurations and consolidating the experiential configuration adaptively.

In tetrapods we see further integration of the CNS and ENS via the limbic and adrenal structures and, in mammals, the emergence of the neocortex and myelinated parasympathetic division.

Behavioral Innovation and Pharyngeal Arch Transformation

Paul D. McLean proposed that the structure of human nervous system is triune as a result of three distinct stages of it´s evolution over time.

McLean proposed the following three stages:

• Reptilian Complex
• Paleomammalian
• Neomammalian

Although throughout the rest of this work I will adapt a triune structure for the nervous system of amniotes and mammals, I call into question the placement of the evolutionary and structural boundaries of the systems as defined by McLean.

Using Alfred Sherwood Romer´s Somato-Visceral Animal, the Polyvagal Theory of Stephen W. Porges and the Dissolution Theory of John Hughlings Jackson as an inspirational guide - I will propose that the triune structure of the brain be directly related to the emergence of central nervous system structures that accompany abrupt changes in the architecture of the autonomic and pharyngeal arch systems.

The evolutionary modifications of the vertebrate nervous system are accompanied by major shifts in the degree behavioral freedom and physiological regulation available to the organism as it operates in realtime.

The pharyngeal arch transitions are often accompanied by parcellation of existing neural structures as well as the emergence of new neural structures - with the neural crest playing an important role in the developmental process of integrating the somatic and visceral bodies together into a functional whole.

There are, at minimum, three distinct stages of evolutionary transformation that are relevant to understanding the subsequent changes in the pharyngeal complex leading from the Pharyngeal-Hindbrain Complex to the anatomy that characterizes the mammalian brainstem:

• The Agnatha-Gnathostome Transformation - Transformation of the 1st pharyngeal arch into jaws and the trigeminal nerve/nuclei in conjunction with the development of myelin, the endocrine system, and sympathetic active arousal systems. This transformation made possible by the emergence of myelin and appendicular fins.


• The Tetrapod-Amniote Transformation - Transition to the cardiopulmonary loop as primary respiration moves from the pharyngeal arches to the lungs. This is accompanied by the emergence of increased complexity in the limbic system and further development of the sympathetic/HPA axial system.


• The Amniote-Mammal Transformation - Transformation of the remaining pharyngeal arch components into the social engagement system of mammals accompanied by the emergence of the cerebral cortex and it´s voluntary motor pathways; as well as, the emergence of the nucleus ambiguous and it´s accompanying myelinated parasympathetic division.

Evolutionary Stage	Somatic Animal (CNS)	Visceral Animal (ENS)
Agnatha (general unmyelinated parasympathetic system only)
Gnathostome (trigeminal and myelinated sympathetic systems)
Tetrapoda (limbic system and adrenal medulla)
Mammals (neocortical structures and myelinated parasympathetic components)	Special myelinated branchial components of the parasympathetic system and cerebral cortex.