Distinct Central Representations of Inescapable and Escapable Pain: Observations and Speculation

It is well established clinically that the affective response to pain of deep origin (muscles, joints and viscera) is distinct from that evoked by cutaneous pain. Cutaneous pain triggers a fight‐flight reaction (active emotional coping), whereas deep pain evokes a reaction of quiescence, decreased vigilance and vasodepression (passive emotional coping). These observations led to suggestions of distinct central representations for deep versus cutaneous pain. Indeed, studies using immediate early gene (c‐fos) expression revealed selective activation of ventrolateral versus lateral columns of the midbrain periaqueductal grey region (PAG) by persistent pain of deep origin versus intermittent cutaneous pain. Ventrolateral versus lateral PAG activation had been found earlier to evoke passive versus active emotional coping. However, not all cutaneous pain triggers active coping. Persistent cutaneous pain (e.g. burns) instead, usually evokes passive coping. This raised the question of whether the behavioural significance of pain (i.e. its escapability versus inescapability), rather than its tissue origin, is represented in supraspinal regions such as the PAG. Subsequent study revealed that a persistent (inescapable) noxious cutaneous manipulation (clip of the neck) evoked both selective ventrolateral PAG Fos expression and passive emotional coping. Such data suggest that pain representation in the PAG reflects a quality akin to behavioural significance, rather than tissue origin. In contrast, in the spinal cord predominantly superficial dorsal horn Fos expression was seen after either persistent or intermittent noxious cutaneous stimuli, leaving the question of the pathway(s) via which persistent (inescapable) cutaneous pain activates the vlPAG unanswered. One experimental approach to this question is suggested.

[1]  A I Basbaum,et al.  Differential origins of spinothalamic tract projections to medial and lateral thalamus in the rat , 1979, The Journal of comparative neurology.

[2]  G. Giesler,et al.  Response properties of neurons of the lateral cervical nucleus in the rat , 1979, The Journal of comparative neurology.

[3]  J. Bonica The relation of injury to pain , 1979, Pain.

[4]  D. Menétrey,et al.  Location and properties of dorsal horn neurons at origin of spinoreticular tract in lumbar enlargement of the rat. , 1980, Journal of neurophysiology.

[5]  A. Fleischmann,et al.  Clip induced analgesia and immobility in the mouse: Activation by different sensory modalities , 1988, Physiology & Behavior.

[6]  D. Menétrey,et al.  Neuropeptides in long ascending spinal tract cells in the rat: Evidence for parallel processing of ascending information , 1988, Neuroscience.

[7]  A. Fleischmann,et al.  Clip-induced analgesia and immobility in the mouse: Pharmacological characterization , 1988, Neuropharmacology.

[8]  A. Fleischmann,et al.  Different endogenous analgesia systems are activated by noxious stimulation of different body regions , 1988, Brain Research.

[9]  A. Fleischmann,et al.  Clip-induced analgesia: Noxious neck pinch suppresses spinal and mesencephalic neural responses to noxious peripheral stimulation , 1989, Physiology & Behavior.

[10]  D. Menétrey,et al.  Expression of c‐fos protein in interneurons and projection neurons of the rat spinal cord in response to noxious somatic, articular, and visceral stimulation , 1989, The Journal of comparative neurology.

[11]  R. Bandler,et al.  Deep and superficial noxious stimulation increases Fos-like immunoreactivity in different regions of the midbrain periaqueductal grey of the rat , 1993, Neuroscience Letters.

[12]  A. Fleischmann,et al.  Tail-pinch induced analgesia and immobility: altered responses to noxious tail-pinch by prior pinch of the neck , 1993, Brain Research.

[13]  R. Bandler,et al.  Convergence of deep somatic and visceral nociceptive information onto a discrete ventrolateral midbrain periaqueductal gray region , 1994, Neuroscience.

[14]  C. Tassorelli,et al.  Systemic nitroglycerin induces Fos immunoreactivity in brainstem and forebrain structures of the rat , 1995, Brain Research.

[15]  R. Bandler,et al.  Columnar organization in the midbrain periaqueductal gray and the integration of emotional expression. , 1996, Progress in brain research.

[16]  R. Bandler,et al.  Common patterns of increased and decreased fos expression in midbrain and pons evoked by noxious deep somatic and noxious visceral manipulations in the rat. , 1996, The Journal of comparative neurology.

[17]  R. Bandler,et al.  Vascular head pain selectively activates ventrolateral periaqueductal gray in the cat , 1998, Neuroscience Letters.

[18]  R. Bandler,et al.  The Neuroanatomy of Cardiac Nociceptive Pathways , 2000 .

[19]  Richard Bandler,et al.  Central circuits mediating patterned autonomic activity during active vs. passive emotional coping , 2000, Brain Research Bulletin.

[20]  R. Bandler,et al.  Muscle pain activates a direct projection from ventrolateral periaqueductal gray to rostral ventrolateral medulla in rats , 2000, Neuroscience Letters.

[21]  J. Price,et al.  Brain mediation of active and passive emotional coping. , 2000, Progress in brain research.

[22]  R. Bandler,et al.  Different representations of inescapable noxious stimuli in the periaqueductal gray and upper cervical spinal cord of freely moving rats , 2001, Neuroscience Letters.