Diffuse optical tomography of pain and tactile stimulation: Activation in cortical sensory and emotional systems

Using diffuse optical tomography (DOT), we detected activation in the somatosensory cortex and frontal brain areas following tactile (brush) and noxious heat stimulation. Healthy volunteers received stimulation to the dorsum of the right hand. In the somatosensory cortex area, tactile stimulation produced a robust, contralateral to the stimulus, hemodynamic response with a weaker activation on the ipsilateral side. For the same region, noxious thermal stimuli produced bilateral activation of similar intensity that had a prolonged activation with a double peak similar to results that have been reported with functional MRI. Bilateral activation was observed in the frontal areas, oxyhemoglobin changes were positive for brush stimulation while they were initially negative (contralateral) for heat stimulation. These results suggest that based on the temporal and spatial characteristics of the response in the sensory cortex, it is possible to discern painful from mechanical stimulation using DOT. Such ability might have potential applications in a clinical setting in which pain needs to be assessed objectively (e.g., analgesic efficacy, pain responses during surgery).

[1]  David Bowsher,et al.  Pain activates cortical areas in the preterm newborn brain , 2006, Pain.

[2]  A. Vania Apkarian,et al.  Abnormal brain chemistry in chronic back pain: an in vivo proton magnetic resonance spectroscopy study , 2000, Pain.

[3]  Jürgen Lorenz,et al.  A Unique Representation of Heat Allodynia in the Human Brain , 2002, Neuron.

[4]  Judith Meek,et al.  Cortical Pain Responses in Human Infants , 2006, The Journal of Neuroscience.

[5]  Karl J. Friston,et al.  Cortical and subcortical localization of response to pain in man using positron emission tomography , 1991, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  H. Handwerker,et al.  Cortical representation of experimental tooth pain in humans , 2005, Pain.

[7]  David Borsook,et al.  Noxious hot and cold stimulation produce common patterns of brain activation in humans: a functional magnetic resonance imaging study , 2000, Neuroscience Letters.

[8]  S. Minoshima,et al.  Cerebral processing of acute skin and muscle pain in humans. , 1997, Journal of neurophysiology.

[9]  David A Boas,et al.  Diffuse optical imaging of the whole head. , 2006, Journal of biomedical optics.

[10]  S. G. Patrick Hardy,et al.  Prefrontal influences upon the midbrain: A possible route for pain modulation , 1985, Brain Research.

[11]  A. Iriki,et al.  Bilateral hand representation in the postcentral somatosensory cortex , 1994, Nature.

[12]  C J Hodge,et al.  The spinothalamic tract. , 1990, Critical reviews in neurobiology.

[13]  Alan C. Evans,et al.  Multiple representations of pain in human cerebral cortex. , 1991, Science.

[14]  V. Andrew Stenger,et al.  Cerebral activation during hypnotically induced and imagined pain , 2004, NeuroImage.

[15]  S. Minoshima,et al.  Keeping pain out of mind: the role of the dorsolateral prefrontal cortex in pain modulation. , 2003, Brain : a journal of neurology.

[16]  Hideshi Shibata,et al.  Organization of anterior cingulate and frontal cortical projections to the anterior and laterodorsal thalamic nuclei in the rat , 2005, Brain Research.

[17]  D. Kleinfeld,et al.  Suppressed Neuronal Activity and Concurrent Arteriolar Vasoconstriction May Explain Negative Blood Oxygenation Level-Dependent Signal , 2007, The Journal of Neuroscience.

[18]  Takeo Ishigaki,et al.  Contralateral and ipsilateral responses in primary somatosensory cortex following electrical median nerve stimulation—an fMRI study , 2005, Clinical Neurophysiology.

[19]  R. Kraft,et al.  Brain Mechanisms Supporting Spatial Discrimination of Pain , 2007, The Journal of Neuroscience.

[20]  R. Peyron,et al.  Functional imaging of brain responses to pain. A review and meta-analysis (2000) , 2000, Neurophysiologie Clinique/Clinical Neurophysiology.

[21]  B. Krauss,et al.  Differentiating cortical areas related to pain perception from stimulus identification: temporal analysis of fMRI activity. , 1999, Journal of neurophysiology.

[22]  Riitta Hari,et al.  Transient Suppression of Ipsilateral Primary Somatosensory Cortex during Tactile Finger Stimulation , 2006, The Journal of Neuroscience.

[23]  W. K. Dong,et al.  Nociceptive responses of neurons in medial thalamus and their relationship to spinothalamic pathways. , 1978, Journal of neurophysiology.

[24]  Nikolaus Weiskopf,et al.  Anterolateral Prefrontal Cortex Mediates the Analgesic Effect of Expected and Perceived Control over Pain , 2006, The Journal of Neuroscience.

[25]  Koji Inui,et al.  Multiple pathways for noxious information in the human spinal cord , 2006, PAIN.

[26]  H. Barbas,et al.  Topographic Organization of Connections between the Hypothalamus and Prefrontal Cortex in the Rhesus Monkey , 2022 .

[27]  R. Treede,et al.  Human brain mechanisms of pain perception and regulation in health and disease , 2005, European journal of pain.

[28]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[29]  Tom Brismar,et al.  Tactile stimulation of the hand causes bilateral cortical activation: a functional magnetic resonance study in humans , 1999, Neuroscience Letters.

[30]  Scott T Reeves,et al.  Postoperative Left Prefrontal Repetitive Transcranial Magnetic Stimulation Reduces Patient-controlled Analgesia Use , 2006, Anesthesiology.

[31]  D. Borsook,et al.  Distinct lateral and medial projections of the spinohypothalamic tract of the rat , 1996, The Journal of comparative neurology.

[32]  M. Bushnell,et al.  Pain perception: is there a role for primary somatosensory cortex? , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[33]  Sachiko Koyama,et al.  Activity in Posterior Parietal Cortex Following Somatosensory Stimulation in Man: Magnetoencephalographic Study Using Spatio-Temporal Source Analysis , 2004, Brain Topography.

[34]  Yu-Tai Tsai,et al.  Contact heat evoked potentials in normal subjects. , 2006, Acta neurologica Taiwanica.

[35]  A Paggi,et al.  Contribution of the corpus callosum to bilateral representation of the trunk midline in the human brain: an fMRI study of callosotomized patients , 2006, The European journal of neuroscience.

[36]  Christian Büchel,et al.  Single trial fMRI reveals significant contralateral bias in responses to laser pain within thalamus and somatosensory cortices , 2003, NeuroImage.

[37]  Jean Pailhous,et al.  Interactions Between Cognitive and Sensorimotor Functions in the Motor Cortex: Evidence from the Preparatory Motor Sets Anticipating a Perturbation , 2004, Reviews in the neurosciences.

[38]  A. Apkarian,et al.  Chronic Back Pain Is Associated with Decreased Prefrontal and Thalamic Gray Matter Density , 2004, The Journal of Neuroscience.

[39]  Quan Zhang,et al.  Coregistered tomographic x-ray and optical breast imaging: initial results. , 2005, Journal of biomedical optics.

[40]  Frank Birklein,et al.  Functional imaging of allodynia in complex regional pain syndrome , 2006, Neurology.

[41]  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.

[42]  Edward E. Smith,et al.  Placebo-Induced Changes in fMRI in the Anticipation and Experience of Pain , 2004, Science.

[43]  H. Breiter,et al.  Reward Circuitry Activation by Noxious Thermal Stimuli , 2001, Neuron.

[44]  J. Maisog,et al.  Pain intensity processing within the human brain: a bilateral, distributed mechanism. , 1999, Journal of neurophysiology.

[45]  Bruce Pike,et al.  Differentiating noxious- and innocuous-related activation of human somatosensory cortices using temporal analysis of fMRI. , 2002, Journal of neurophysiology.

[46]  Matthew T. Sutherland,et al.  Reliable detection of bilateral activation in human primary somatosensory cortex by unilateral median nerve stimulation , 2006, NeuroImage.

[47]  Christian Maihöfner,et al.  Neural activation during experimental allodynia: a functional magnetic resonance imaging study , 2004, The European journal of neuroscience.

[48]  H. Breiter,et al.  Human brain activation under controlled thermal stimulation and habituation to noxious heat: An fMRI study , 1999, Magnetic resonance in medicine.

[49]  M. L. Wood,et al.  fMRI of human somatosensory and cingulate cortex during painful electrical nerve stimulation , 1995, Neuroreport.

[50]  Leah Krubitzer,et al.  Interhemispheric connections of somatosensory cortex in the flying fox , 1998, The Journal of comparative neurology.

[51]  J. Kaas,et al.  The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys , 1983, The Journal of comparative neurology.

[52]  S. Aalto,et al.  Effects of Surgical Levels of Propofol and Sevoflurane Anesthesia on Cerebral Blood Flow in Healthy Subjects Studied with Positron Emission Tomography , 2002, Anesthesiology.

[53]  Toshifumi Kumai,et al.  Face area representation of primary somatosensory cortex in humans identified by whole-head magnetoencephalography. , 2004, The Japanese journal of physiology.

[54]  D. Boas,et al.  Hemodynamic evoked response of the sensorimotor cortex measured noninvasively with near-infrared optical imaging. , 2003, Psychophysiology.

[55]  David Borsook,et al.  Trigeminal Neuropathic Pain Alters Responses in CNS Circuits to Mechanical (Brush) and Thermal (Cold and Heat) Stimuli , 2006, The Journal of Neuroscience.

[56]  B L Whitsel,et al.  Response of anterior parietal cortex to different modes of same-site skin stimulation. , 1998, Journal of neurophysiology.

[57]  T. Wilcox,et al.  Using near-infrared spectroscopy to assess neural activation during object processing in infants. , 2005, Journal of biomedical optics.

[58]  Peter Svensson,et al.  A PET activation study of brush-evoked allodynia in patientswith nerve injury pain , 2006, Pain.

[59]  H. Barbas Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices , 2000, Brain Research Bulletin.