BRAIN ACTIVATION RELATED TO AFFECTIVE DIMENSION DURING THERMAL STIMULATION IN HUMANS: A FUNCTIONAL MAGNETIC RESONANCE IMAGING STUDY

The aim of this study was to identify the activated brain region that is involved with the affective dimension of thermal stimulation (not pain, but innocuous warming) using functional MR imaging. Twelve healthy, right-handed male subjects participated in the study. Thermal stimulation with two different temperatures of 41°C and 34°C was applied to the subjects using a fomentation pack, wrapped around the right lower leg of each subject. On the basis of the subjects’ responses after the scanning sessions, the authors were able to observe that the subjects felt “warm” and “slightly pleasant and comfortable” under the 41°C condition. The experimental results indicated that warm stimulation produced a significant increase of activation compared to thermal neutral stimulation in various regions such as contralateral insular, ipsilateral cerebellum, ipsilateral putamen, contralateral middle frontal gyrus, ipsilateral inferior frontal gyrus, contralateral postcentral gyrus, and contralateral paracentral lobule. The activated regions are known to be related to thermal sensory, affective/emotional awareness, cognitive functions, sensory-discrimination, and emotion/affective processing, and so on. These results suggest that an appropriate thermal stimulation can produce a positive emotion and activate emotion/affect related regions of the brain.

[1]  P. Roland,et al.  Bilateral activation of fronto-parietal networks by incrementing demand in a working memory task. , 1997, Cerebral cortex.

[2]  Albert Gjedde,et al.  Origin of Human Motor Readiness Field Linked to Left Middle Frontal Gyrus by MEG and PET , 1998, NeuroImage.

[3]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[4]  A. Craig.  A new view of pain as a homeostatic emotion , 2003, Trends in Neurosciences.

[5]  R. Koeppe,et al.  Comparison of human cerebral activation pattern during cutaneous warmth, heat pain, and deep cold pain. , 1996, Journal of neurophysiology.

[6]  J. Lewin,et al.  Cortical localization of human sustained attention: detection with functional MR using a visual vigilance paradigm. , 1996, Journal of computer assisted tomography.

[7]  Vinod Goel,et al.  Neuroanatomical Correlates of Human Reasoning , 1998, Journal of Cognitive Neuroscience.

[8]  Y. Miyashita,et al.  Common inhibitory mechanism in human inferior prefrontal cortex revealed by event-related functional MRI. , 1999, Brain : a journal of neurology.

[9]  D. Cechetto,et al.  Autonomic responses and efferent pathways from the insular cortex in the rat , 1991, The Journal of comparative neurology.

[10]  Mark S. Cohen,et al.  Changes in cortical activity during mental rotation. A mapping study using functional MRI. , 1996, Brain : a journal of neurology.

[11]  Y. Okamoto,et al.  Brain activity during expectancy of emotional stimuli: an fMRI study , 2003, Neuroreport.

[12]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[13]  A. Young,et al.  Face processing impairments after amygdalotomy. , 1997, Brain : a journal of neurology.

[14]  Norihiro Sadato,et al.  Brain activation during whole body cooling in humans studied with functional magnetic resonance imaging , 2002, Neuroscience Letters.

[15]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[16]  L. Becerra,et al.  CNS activation by noxious heat to the hand or foot: site-dependent delay in sensory but not emotion circuitry. , 2004, Journal of neurophysiology.

[17]  J C Gore,et al.  Functional MR imaging of regional brain activation associated with the affective experience of pain. , 2001, AJR. American journal of roentgenology.

[18]  A. Nakamura,et al.  Vocal identification of speaker and emotion activates differerent brain regions , 1997, Neuroreport.

[19]  Alan C. Evans,et al.  Functional imaging of an illusion of pain , 1996, Nature.

[20]  C Büchel,et al.  Somatotopic representation of nociceptive information in the putamen: an event-related fMRI study. , 2004, Cerebral cortex.

[21]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[22]  H. Hensel.  Thermoreception and temperature regulation. , 1981, Monographs of the Physiological Society.

[23]  R. Adolphs,et al.  Fear and the human amygdala , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  P. Roland,et al.  Right prefrontal activation during encoding, but not during retrieval, in a non-verbal paired-associates task. , 1998, Cerebral cortex.

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

[26]  R. Coghill,et al.  Hemispheric lateralization of somatosensory processing. , 2001, Journal of neurophysiology.

[27]  G. McCarthy,et al.  Dissociable prefrontal brain systems for attention and emotion , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[28]  R. E. Wheeler,et al.  Individual differences in anterior brain asymmetry and fundamental dimensions of emotion. , 1992, Journal of personality and social psychology.

[29]  Neuropsychology. Modulation by instruction. , 1995, Nature.

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

[31]  S. Hamann,et al.  Positive and negative emotional verbal stimuli elicit activity in the left amygdala , 2002, Neuroreport.

[32]  D. Brooks,et al.  Evidence for striatal dopamine release during a video game , 1998, Nature.

[33]  A. D. Craig,et al.  Human feelings: why are some more aware than others? , 2004, Trends in Cognitive Sciences.

[34]  Albert Gjedde,et al.  Cortical Sites of Sustained and Divided Attention in Normal Elderly Humans , 1997, NeuroImage.

[35]  P. Goldman-Rakic,et al.  Human Brain Mapping 6:14–32(1998) � Dissociation of Mnemonic and Perceptual Processes During Spatial and Nonspatial Working Memory Using fMRI , 2022 .

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

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

[38]  Sophie K. Scott,et al.  Impaired auditory recognition of fear and anger following bilateral amygdala lesions , 1997, Nature.

[39]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[40]  S J Bolanowski,et al.  Heat-induced pain diminishes vibrotactile perception: a touch gate. , 1994, Somatosensory & motor research.

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

[42]  S. Taylor,et al.  The Effect of Emotional Content on Visual Recognition Memory: A PET Activation Study , 1998, NeuroImage.

[43]  J. Allen.  Human Physiology - the Basis of Medicine , 2008, The Ulster Medical Journal.

[44]  S. Zeki,et al.  The neural basis of romantic love , 2000, Neuroreport.

[45]  C. L. Kwan,et al.  Functional MRI study of thalamic and cortical activations evoked by cutaneous heat, cold, and tactile stimuli. , 1998, Journal of neurophysiology.

[46]  Hanna Damasio,et al.  Premotor and Prefrontal Correlates of Category-Related Lexical Retrieval , 1998, NeuroImage.

[47]  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.

[48]  J. Desmond,et al.  Dissociation of Frontal and Cerebellar Activity in a Cognitive Task: Evidence for a Distinction between Selection and Search , 1998, NeuroImage.

[49]  Michael Posner,et al.  Modulation by instruction , 1995, Nature.

[50]  Gregory P. Lee,et al.  Neural Substrates of Emotion as Revealed by Functional Magnetic Resonance Imaging , 2004, Cognitive and behavioral neurology : official journal of the Society for Behavioral and Cognitive Neurology.

[51]  M Jeannerod,et al.  Visual working memory for shape and 3D‐orientation: a PET study , 1997, Neuroreport.

[52]  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.

[53]  J. R. Augustine.  Circuitry and functional aspects of the insular lobe in primates including humans , 1996, Brain Research Reviews.