Is there a specific lamina I spinothalamocortical pathway for pain and temperature sensations in primates?

We welcome the opportunity to comment on the critical review by Willis et al. In the following, we address a few major issues raised in their article, and then we comment specifically on our identification of VMpo in human thalamus. The focus article by Willis et al reflects their broad familiarity with the literature. The first author, WD Willis, performed the initial, classic identification of primate spinothalamic (STT) neurons with antidromic activation and natural stimulation, and his book reviewing experimental work on pain was a milestone in the field that deserves enduring respect. However, the currently available findings do not support the arguments of Willis et al, and we believe the evidence indicates a view of ascending pain pathways that is conceptually distinct from their view, as we will point out.

[1]  A. Craig.  The functional anatomy of lamina I and its role in post-stroke central pain. , 2000, Progress in brain research.

[2]  W. Willis,et al.  Responses of primate spinothalamic neurons to graded and to repeated noxious heat stimuli. , 1979, Journal of neurophysiology.

[3]  J. Dostrovsky,et al.  Thalamic relay site for cold perception in humans. , 1999, Journal of neurophysiology.

[4]  B L Whitsel,et al.  Anterior parietal cortical response to tactile and skin-heating stimuli applied to the same skin site. , 1996, Journal of neurophysiology.

[5]  E. Carstens.  Responses of rat spinal dorsal horn neurons to intracutaneous microinjection of histamine, capsaicin, and other irritants. , 1997, Journal of neurophysiology.

[6]  G. Leijon,et al.  Central post-stroke pain — a study of the mechanisms through analyses of the sensory abnormalities , 1989, Pain.

[7]  R HASSLER,et al.  [Anatomy of the thalamus]. , 1950, Archiv fur Psychiatrie und Nervenkrankheiten, vereinigt mit Zeitschrift fur die gesamte Neurologie und Psychiatrie.

[8]  C. Saper,et al.  Calcitonin gene‐related peptide immunoreactivity in the visceral sensory cortex, thalamus, and related pathways in the rat , 1989, The Journal of comparative neurology.

[9]  E. Perl,et al.  Spinal neurons specifically excited by noxious or thermal stimuli: marginal zone of the dorsal horn. , 1970, Journal of neurophysiology.

[10]  L. Krubitzer,et al.  Somatotopic organization of cortical fields in the lateral sulcus of Homo sapiens: Evidence for SII and PV , 2000, The Journal of comparative neurology.

[11]  W. Willis,et al.  Neuroanatomy of the pain system and of the pathways that modulate pain. , 1997, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[12]  A. Blomqvist.  Gracilo‐diencephalic relay cells: A quantitative study in the cat using retrograde transport of horseradish peroxidase , 1980, The Journal of comparative neurology.

[13]  J. Gybels,et al.  Positron emission tomography study of a chronic pain patient successfully treated with somatosensory thalamic stimulation , 2000, Pain.

[14]  W. Willis,et al.  A critical review of the role of the proposed VMpo nucleus in pain. , 2002, The journal of pain : official journal of the American Pain Society.

[15]  A. Craig,et al.  Spinothalamic lamina I neurons selectively sensitive to histamine: a central neural pathway for itch , 2001, Nature Neuroscience.

[16]  William D. Willis,et al.  Responses of primate spinothalamic tract neurons to natural stimulation of hindlimb. , 1974 .

[17]  A. Craig,et al.  Cytoarchitectonic and immunohistochemical characterization of a specific pain and temperature relay, the posterior portion of the ventral medial nucleus, in the human thalamus. , 2000, Brain : a journal of neurology.

[18]  William D. Willis,et al.  The cells of origin of the primate spinothalamic tract , 1979, The Journal of comparative neurology.

[19]  H. Ralston,et al.  The primate dorsal spinothalamic tract: evidence for a specific termination in the posterior nuclei (Po/SG) of the thalamus , 1992, Pain.

[20]  W. Mehler.  The posterior thalamic region in man. , 1966, Confinia neurologica.

[21]  W. Willis,et al.  Projections from the marginal zone and deep dorsal horn to the ventrobasal nuclei of the primate thalamus , 2001, Pain.

[22]  B L Whitsel,et al.  Characteristics of temporal summation of second pain sensations elicited by brief contact of glabrous skin by a preheated thermode. , 1997, Journal of neurophysiology.

[23]  E. Perl.  Why are Selectively Responsive and Multireceptive Neurons both Present in Somatosensory Pathways , 1984 .

[24]  HJ Ralston,et al.  Medial lemniscal and spinal projections to the macaque thalamus: an electron microscopic study of differing GABAergic circuitry serving thalamic somatosensory mechanisms , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  A. Craig.  Spinal location of ascending lamina I axons in the macaque monkey , 2000 .

[26]  M. Bushnell,et al.  A thalamic nucleus specific for pain and temperature sensation , 1994, Nature.

[27]  A. Craig,et al.  A distinct thermoreceptive subregion of lamina I in nucleus caudalis of the owl monkey , 1999, The Journal of comparative neurology.

[28]  A Schnitzler,et al.  Pain affect without pain sensation in a patient with a postcentral lesion , 1999, Pain.

[29]  E. G. Jones,et al.  A new parcellation of the human thalamus on the basis of histochemical staining , 1989, Brain Research Reviews.

[30]  A. Craig,et al.  Evidence for glutamate as a neurotransmitter in spinothalamic tract terminals in the posterior region of owl monkeys , 1996, Experimental Brain Research.

[31]  E. Reiman,et al.  Thermosensory activation of insular cortex , 2000, Nature Neuroscience.

[32]  I. Tracey,et al.  Cortical Processing of Human Somatic and Visceral Sensation , 1999, The Journal of Neuroscience.

[33]  W. Willis,et al.  Responses of primate spinothalamic neurons located in the sacral intermediomedial gray (stilling's nucleus) to proprioceptive input from the tail , 1982, Brain Research.

[34]  R. Dubner,et al.  Spatial and temporal transformations of input to spinothalamic tract neurons and their relation to somatic sensations. , 1978, Journal of neurophysiology.

[35]  J. Schouenborg,et al.  A survey of spinal dorsal horn neurones encoding the spatial organization of withdrawal reflexes in the rat , 2004, Experimental Brain Research.

[36]  Frank Munz,et al.  Central activation by histamine-induced itch: analogies to pain processing: a correlational analysis of O-15 H2O positron emission tomography studies , 2001, Pain.

[37]  A. Morel,et al.  Multiarchitectonic and stereotactic atlas of the human thalamus , 1997, The Journal of comparative neurology.

[38]  H. Burton,et al.  The posterior thalamic region and its cortical projection in new world and old world monkeys , 1976, The Journal of comparative neurology.

[39]  Fred A Lenz,et al.  Pain sensitivity alterations as a function of lesion location in the parasylvian cortex , 1999, Pain.

[40]  J. Gybels,et al.  Neurosurgical treatment of persistent pain. Physiological and pathological mechanisms of human pain. , 1989, Pain and headache.

[41]  W. Miltner,et al.  Dipole analysis of ultralate (C-fibres) evoked potentials after laser stimulation of tiny cutaneous surface areas in humans , 2001, Neuroscience Letters.

[42]  M. Bushnell,et al.  Cortical representation of the sensory dimension of pain. , 2001, Journal of neurophysiology.

[43]  H. Freund,et al.  Differential organization of touch and pain in human primary somatosensory cortex. , 2000, Journal of neurophysiology.

[44]  W. Willis,et al.  Natural groupings of primate spinothalamic neurons based on cutaneous stimulation. Physiological and anatomical features. , 1988, Journal of neurophysiology.