Integrated Prescriptive Pain Theories

Several theoretical frameworks have been proposed to explain the physiological basis of pain, although none yet completely accounts for all aspects of pain perception. Here, we provide a historical overview of the major contributions, ideas, and competing theories of pain from ancient civilizations to Melzack and Wall’s Gate Control Theory of Pain.

The current definition of pain, established by the International Association for the Study of Pain (IASP) in 1986, defines pain as “an unpleasant sensory and emotional experience associated with actual or potential tissue damage, or described in terms of tissue damage, or both.” This definition is the culmination of centuries of ideas and work that have explored the concept of pain.

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A number of theories have been postulated to describe mechanisms underlying pain perception. These theories date back several centuries and even millennia (Kenins 1988; Perl 2007; Rey 1995). This review will mainly focus on theories postulated since the 17th century and then provide an overview of current thinking. The four most influential theories of pain perception include the Specificity (or Labeled Line), Intensity, Pattern, and Gate Control Theories of Pain (Fig. 1)Integrated Prescriptive Pain Theories.

SPECIFICITY THEORY OF PAIN

The Specificity Theory refers to the presence of dedicated pathways for each somatosensory modality. The fundamental tenet of the Specificity Theory is that each modality has a specific receptor and associated sensory fiber (primary afferent) that is sensitive to one specific stimulus (Dubner et al. 1978). For instance, the model proposes that non-noxious mechanical stimuli are encoded by low-threshold mechanorecepetors, which are associated with dedicated primary afferents that project to “mechanoreceptive” second-order neurons in the spinal cord or brainstem (depending on the source of the input). These second-order neurons project to “higher” mechanoreceptive areas in the brain. Similarly, noxious stimuli would activate a nociceptor, which would project to higher “pain” centers through a pain fiber. These ideas have been emerging over several millennia but were experimentally tested and formally postulated as a theory in the 19th century by physiologists in Western Europe.

Descartes’ description of the pain system.

René Descartes was one of the first Western philosophers to describe a detailed somatosensory pathway in humans. Descartes’ manuscript, Treatise of Man (originally written in French), was illustrated, edited, and published posthumously, first in Latin in 1662 (Descartes 1662) and then in French in 1664 (Descartes et al. 1664). In Treatise of Man, based on the French edition by Louis La Forge (who was also one of the illustrators), Descartes describes pain as a perception that exists in the brain and makes the distinction between the neural phenomenon of sensory transduction (today, known as nociception) and the perceptual experience of pain. What is essential to the development of Descartes’ theory is his description of nerves, which he perceived as hollow tubules that convey both sensory and motor information. This understanding of neural function was by no means novel. In the third century BCE, Herophilus demonstrated the existence of sensory and motor nerves, and Erasistratus demonstrated that the brain influenced motor activity (Rey 1995). One-half of a millennium later, Galen demonstrated that sectioning the spinal cord caused sensory and motor deficits (Ochs 2004). Within the spirit of scientific enquiry that resurfaced in the renaissance, anatomical studies by Vesalius published in 1543 reiterated and confirmed Galen’s findings (Ochs 2004)Integrated Prescriptive Pain Theories. In relation to this, Galen had postulated that three conditions be met for perception: 1) an organ must be able to receive the stimulus, 2) there must be a connection from the organ to the brain, and 3) a processing center that converts the sensation to a conscious perception must exist (Rey 1995). Descartes contributed to Galen’s model by postulating that a gate existed between the brain and the tubular structures (the connections), which was opened by a sensory cue (Descartes et al. 1664). A sensory cue would “tug” on the tube, which would then open a gate between the tube and the brain. The opening of this gate would then allow “animal spirits” (an extension of the Greek pneuma¹) to flow through these tubes and within the muscles to move them. Although this sensory system was not specific to pain, La Forge’s drawing (based on Descartes’ concept and La Forge’s understanding of contemporaneous anatomy) of a foot near a flame is one of the most famous figures in neuroscience (Fig. 2). This example describes the pathway for promptly moving one’s foot away from a hot flame. In the figure (and its description in the text), the heat of the flame near the foot activates a fibril (or fiber) within the nerve tubule that traverses up the leg, to the spinal cord, and finally, to the brain. Descartes compared this fiber with a cord attached to a bell—by pulling on the other end of cord, the bell will ring. The proverbial bells, in this case, are the pores that line the ventricles in the brain. Once these pores open in response to the sensory input, the animal spirits were thought to flow through the tubule and elicit a motor response. This motor response included turning the head and the eyes to see the flame and raising the hands and folding the body away from the flame for protection. Descartes conceived that there are many of these fibrils and that their movements elicit the sensations. For example, the perception of pain would be felt in the brain when there is a significant tug on the fiber, which caused it to sever. In contrast, a tug of the same magnitude that does not cause the fiber to break would evoke a tickling (or tingling; Descartes uses the French word chatouillement) perception. Although La Forge’s figure of the boy and the flame suggests that there is a dedicated pain pathway, a closer read of the text indicates that Descartes believed that the pattern and rate of firing (intensity of tugging) of a fiber provided the adequate information to the brain about the stimulus intensity and quality. In fact, it is likely that the misconception of a dedicated pathway in the somatosensory system by Descartes is an extension of his proposal that the visual system requires a labeled line (where the image is carried and projected in the brain)Integrated Prescriptive Pain Theories.