Atkinson Pain Research Laboratory

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Atkinson Pain Research Laboratory


A. D. "Bud" Craig, PhD
Principal Investigator


Laboratory Focus

 
 A. D. "Bud" Craig, PhD

In the Atkinson Pain Research Laboratory, we study connections from the spinal cord to the brain that are involved in "feelings" from the body. The main connection originates in a spinal region called lamina I. Quantitative analyses of lamina I spinothalamic neurons indicate that they serve as "labeled lines" that generate sharp pain, burning pain, warm, cool, itch, muscle ache, sensual touch and other sensations related to the body's physiological condition. Anatomic work in the laboratory shows that lamina I neurons project their axons first to autonomic spinal and homeostatic brainstem regions, then to a specific thalamocortical relay nucleus called VMpo, found only in primates and greatly enlarged in humans, which projects in turn to posterior insular cortex. This pathway contains sensory input from regions of the body that are innervated by sympathetic efferents.

Our work has shown that stimulation of sensory fibers in the parasympathetic vagus nerve produces activity within a parallel homeostatic afferent pathway in primates. Together these two pathways provide a complete representation of the sensory condition of all tissues of the body. These findings led to the novel concept that the affective feelings from the body constitute a sense of the body's physiologic condition, which we call interoception. This concept suggests that pain can be viewed as a reflection of the homeostatic processes in the brain that evolved to maintain the body's health, that is, a homeostatic emotion. Feelings of pain indicate that there is something wrong in the body that the autonomic nervous system cannot rectify on its own.

Further work suggests that re-representations of this interoceptive sensory pathway that are integrated with motivational states and social context provide the neuroanatomical foundation for subjective human awareness of the material (sentient) self. This concept converges with the neurological concept that conscious human emotions are based on "somatic markers" that represent the homeostatic condition of the body, a modern extension of the James-Lange theory of emotion. These neuroanatomical findings provide a substantive foundation for human awareness. This perspective provides a new paradigm for explaining interactions of pain with emotion and homeostatic processing that leads to new ideas for therapeutic intervention.

Current work in the laboratory addresses the integration of pain, temperature, itch and visceral representations within the insular cortex of the primate; the role of the medial thalamus and anterior cingulate cortex in the inhibition of pain by cooling; the association of deep dorsal horn cells with sensorimotor integration (considered for more than 30 years to be pain cells by others); and the characterization of lamina I spinobulbar neurons involved in brainstem homeostatic mechanisms. Further, we are working to elucidate the unique characteristics of the human insula that underpin its hypothesized role in subjective awareness and emotional regulation.

 

 

Laboratory Accomplishments

  • Physiological demonstrations that lamina I spinothalamic neurons constitute distinct "labeled lines" for the sensations referred to as first and second pain, itch, warm, cool, and muscle ache
  • Anatomical demonstrations that lamina I spinothalamic axons can be identified in human spinal cord as the "lateral spinothalamic tract," where cordotomy lesions produce analgesia and thermanesthesia in patients
  • Physiological explanation of the thermal grill illusion of pain, which demonstrates that nonpainful cooling inhibits burning pain within the brain
  • Use of the thermal grill in a multiple sclerosis patient to obtain evidence supporting our theory that central pain is a disinhibitory thermoregulatory syndrome
  • Anatomic, ultrastructural, and physiologic demonstrations that VMpo is a specific relay nucleus for pain and temperature sensations to the insular cortex
  • Publication of the novel concept that pain is a homeostatic emotion
  • Publication of the fundamental neuroanatomical hypothesis that human subjective awareness is based on a cortical re-representation of the interoceptive state of the body engendered in the anterior insula
  • Publication of a neuroanatomical proposal for the forebrain asymmetry of emotion based on lateralized integration of sympathetic activity in the right insula and parasympathetic activity in the left insula

 

Selected Publications

  1. Craig, AD. How do you feel—now? The anterior insula and human awareness. Nat Rev Neurosci. 2009;10: 59-70.

  2. Craig, AD. Retrograde analyses of spinothalamic projections in the macaque monkey: input to the ventral lateral nucleus. J Comp Neurol. 2008;508: 315-328.

  3. Craig, AD. Forebrain emotional asymmetry: a neuroanatomical basis? Trends Cognit Sci. 2005;9:566-571.

  4. Craig, AD. Distribution of trigemino- and spino-thalamic lamina I terminations in the macaque monkey. J Comp Neurol. 2004;477: 119-148.

  5. Craig, AD. A new view of pain as a homeostatic emotion. Trends Neurosci. 2003 Jun;26: 303-307.

  6. Craig, AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci. 2002 Aug; 3: 655-666.

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