While the sparse innervation of internal organs (60) and the widespread divergence of visceral afferents in the central nervous system (CNS) explain the dull, vague, and not well-localized nature of the first phase of a visceral pain sensation (5), the referral of visceral sensations to areas of the body away from the injured organ has always been interpreted as the consequence of convergence of somatic and visceral afferent information onto the same sensory neurons. The rationale for this interpretation is that the brain receives information from both internal organs and somatic areas through the same sensory channel and attributes the origin of the sensation to the somatic domain.
There are two major assumptions in this interpretation. The first one is that the brain locates the origin of a sensory stimulus through a direct sensory channel—a string is pulled at one end and a bell rings at the other telling the brain where the string has been pulled. We now know that things are not so simple and that parallel processing through various specific and nonspecific sensory channels is more likely to mediate a complex painful experience. The second assumption is that the brain will always attribute the origin of a stimulus to a somatic location even when the point stimulated is in the viscera. In other words, regardless of how a convergent sensory pathway is activated—by its somatic or visceral inputs—the final result is always a sensation felt in the somatic region. This assumption implies that somatic locations have a priority over visceral ones when it comes to the assessment by the brain of the origin of a given stimulus. This interpretation of the neural mechanisms of referred pain is based on the principle that sensory perceptions are shaped by a learning process. When a viscerosomatic convergent pathway is activated, the brain attributes the origin of the stimulus to the region, which is the most frequent source of sensory experiences, that is, the somatic area.
Two models of viscerosomatic convergence have been put forward to explain referred visceral pain: a peripheral model of dichotomizing primary afferent fibers and a central model of viscerosomatic convergence onto second-order neurons in the CNS. Both are supported by experimental evidence, although the CNS model is by far the most popular and the one that has received the greatest experimental support.
The peripheral model of viscerosomatic convergence is based on the existence of primary afferent neurons with cell bodies in the dorsal root ganglia (DRG) and whose peripheral projections have several branches with separate endings in internal organs and in somatic structures. In this way, the same primary sensory neuron will have receptive endings in somatic and visceral tissues. Such DRG neurons have been described in several species using anatomical and electrophysiological methods (51,61-64), suggesting that dichotomizing afferent fibers could mediate referred sensations from a variety of viscera including the heart, the GI tract, and the reproductive organs. On the other hand, these reports have also met with some skepticism from alternative studies of dichotomizing afferents showing that, although such afferents can sometimes be observed anatomically or electrophysiological^, their very low numbers (less than 1% of the total number of afferents) make them unlikely candidates as mediators of referred visceral pain (65-67). It is also not known if the sensory endings of such dichotomizing afferents are functionally active in all their various locations and if so, whether all the endings have similar receptive properties (mechanical, thermal, chemical, etc.).
The second model of viscerosomatic convergence is based on the existence of second order neurons in the spinal cord and of other CNS neurons in sensory pathways that receive convergent inputs from somatic and visceral tissues. This interpretation forms the basis of the Convergence-Projection theory of referred visceral pain put forward by Ruch in 1946. The rationale of the theory is that viscerosomatic convergent neurons, when activated by afferent impulses from the viscera, send information to the brain that is interpreted as coming from the somatic areas. The pattern of referral will be determined by the pattern of viscerosomatic convergence so that, for example, if neurons with inputs from cardiac nociceptors have receptive fields in the left thorax and left arm, the pain will be felt in these regions of the body rather than in the heart.
There is considerable experimental evidence in support of this interpretation. Numerous studies have described viscerosomatic convergent neurons in the spinal cord and other regions of the CNS (68-73). The patterns of viscerosomatic convergence from a given organ coincide with the zones of referred visceral pain from the same organ in humans (Fig. 3) and with the somatic areas in experimental animals, which generate behavioral nociceptive patterns (41). Moreover, the fact that viscerosomatic convergence occurs on CNS sensory neurons offers the possibility of substantial integration and modulation at each synaptic relay and therefore a likely substrate for more complex sensory experiences than those mediated exclusively by primary afferents.
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