Neuroanatomy Of Visceral Pain

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Basic science studies have demonstrated that from the level of gross anatomy to the microscopic determination of both peripheral and central afferent terminals, visceral sensory pathways are diffusely organized and distributed (diagrammatic summary in Fig. 1). Rather than mimicking the precise organization of cutaneous sensory afferent pathways, which travel in defined peripheral nerves and extend into a limited number of spinal segmental nerves organized in a unilateral, somatotopic fashion, visceral sensory afferent nerve fibers originate from multiple branchings of nerve fascicles organized into weblike plexuses scattered through the thoracic and abdominal cavities that extend from the prevertebral region to reach the viscera by predominantly perivascular routes. Injection of neuronal tracing agents into focal sites within viscera may easily result in the labeling of cell bodies in the dorsal root ganglia of 10 or more spinal levels in a bilaterally distributed fashion (27). The central spinal projections of visceral afferent neurons have been demonstrated by Sugiura et al. (28) to branch within the spinal cord and to spread over multiple spinal segments located both rostral and caudal to the level of entry. In these studies, individual C-fiber cutaneous afferents were demonstrated to form tight "baskets" of input to the superficial laminae of localized spinal cord segments, but individual C-fiber visceral afferents were demonstrated to terminate in superficial and deep laminae bilaterally in more than 10 spinal segments. Visceral afferents have also been noted to be neurochemically different than cutaneous afferents, with the expression of differing receptor subtypes for chemical stimuli (29).

Visceral sensory processing is uniquely different from cutaneous sensory processing in that there are peripheral sites of the visceral neuronal synaptic contact that occurs with the cell bodies of prevertebral ganglia such as the celiac ganglion, superior mesenteric ganglion, and

Thalamus

Thalamus

Cord

Figure 1 Diagrammatic representation of visceral and superficial pain pathways. Visceral pain pathways are much more diffuse, with multiple peripheral branchings, pathways through prevertebral ganglia, and the sympathetic chain to cell bodies residing bilaterally within multiple dorsal root ganglia. Central projections of visceral afferents also demonstrate significant branching to interact with spinal cord dorsal horn neurons in multiple laminae of multiple spinal segments. Major projections of these dorsal horn neurons to supraspinal structures then travel via dorsal column and ventrolateral quadrant pathways. Superficial pain pathways are, in contrast, much more organized, with distinct peripheral nerves, a limited number of spinal segmental sites of entry, and focal, heavy interaction with a limited number of dorsal horn neurons. Supraspinal connections of these dorsal horn neurons travel predominantly in the ventrolateral quadrant.

Cord

Figure 1 Diagrammatic representation of visceral and superficial pain pathways. Visceral pain pathways are much more diffuse, with multiple peripheral branchings, pathways through prevertebral ganglia, and the sympathetic chain to cell bodies residing bilaterally within multiple dorsal root ganglia. Central projections of visceral afferents also demonstrate significant branching to interact with spinal cord dorsal horn neurons in multiple laminae of multiple spinal segments. Major projections of these dorsal horn neurons to supraspinal structures then travel via dorsal column and ventrolateral quadrant pathways. Superficial pain pathways are, in contrast, much more organized, with distinct peripheral nerves, a limited number of spinal segmental sites of entry, and focal, heavy interaction with a limited number of dorsal horn neurons. Supraspinal connections of these dorsal horn neurons travel predominantly in the ventrolateral quadrant.

pelvic ganglion. This synaptic contact can lead to alterations in local visceral function that is outside of central control. The gut also carries the enteric nervous system as a self-contained "little brain'' regulating the complex functions of digestion/absorption.

The location of the dorsal root ganglion neurons innervating the viscera appears to follow the original location of the structural precursors of the viscera during embryological development. Thoracic organs arose near somites corresponding to thoracic segments. Most abdominal organs arose near somites corresponding to mid-to-low thoracic and upper lumbar spinal segmental structures. Organization appears more complicated in the realm of urogenital/pelvic structures, where a dual innervation is apparent with afferents from lower thoracic-upper lumbar segments and from sacral segments. The testes and ovaries both originate relatively high in the abdomen and so carry with them a thoracic innervation. The urinary bladder arises from structures that traverse the developing umbilicus and is still connected to it by the residual urachus. It has a similar thoracolumbar innervation, with sensory inputs extending up to the T10 level. However, like all structures that physically open their orifices to sacral dermatomes (rectum, genital structures), it also has a dual spinal innervation that includes local sacral inputs (the pelvic nerve; S2-S4). An apparent "gap" in the innervation of urogenital structures is simply the absence of those nerves associated with the hindlimb bud (L3-S1). Mixed with spinal innervations are the wandering inputs and outputs of the vagus nerve and an elaborate local ganglionic circuitry. The result is that pelvic organs such as the urinary bladder, gynecological structures, and the lower gastrointestinal (GI) tract have a complex and doubly diffuse neuroanatomy. Taken together, from a macro- to microscopic level, there is an imprecise and diffuse organization of visceral primary inputs that would be sufficient to explain the imprecise and diffuse localization of visceral events by the central nervous system. However, upon entering the central nervous system, additional mechanisms are at work that lead to additional impreciseness. When quantitatively examined, spinal dorsal horn neurons with visceral inputs have multiple, convergent inputs from other viscera, from joints, from muscle, and from cutaneous structures. This presents a substrate that may explain the phenomenon of referred pain as a misinterpretation of spinal dorsal horn neuronal activity as being due to input from other more commonly activated structures, but it also means that the convergence of inputs from multiple viscera onto the same spinal neurons further contributes to the impreciseness of the localization of the source of pain, since activity in these neurons could reflect visceral, myofascial, articular, or cutaneous pathology. In contrast, neurons with exclusively cutaneous input are commonly identified in the spinal dorsal horn, in particular from nonhairy skin. As such, there is no ambiguity associated with the activation of these neurons and a higher order "interpretation" of their activity.

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