Brain activation during whole body cooling in humans studied with functional magnetic resonance imaging

Kanosue, Kazuyuki; Sadato, Norihiro; Okada, Tomohisa; Yoda, Teruhiko; Nakai, Seiichi; Yoshida, Kyoko; Hosono, Takayoshi; Nagashima, Kei; Yagishita, Tomoko; Ito, Osamu; Kobayashi, Keiko; Yonekura, Yoshiharu

doi:10.1016/s0304-3940(02)00621-3

Cited by 65 publications

(64 citation statements)

References 11 publications

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“…The identification of thermosensory activation in this region of the dorsal medial cortex [which many reviewers nevertheless view as associated with "cognitive," rather than "emotional," behavior (40)] is a second major result of this study. Direct examinations of thermoregulatory processing by other physiologists have not yet identified this region, but further work is clearly needed (31).…”

Section: Discussionmentioning

confidence: 99%

Anteroposterior somatotopy of innocuous cooling activation focus in human dorsal posterior insular cortex

Hua¹,

Strigo²,

Baxter³

et al. 2005

American Journal of Physiology-Regulatory, Integrative and Comp

113

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Prior data indicate that graded activation by innocuous thermal stimuli occurs in the dorsal posterior insular (dpIns) cortex of humans, rather than the parietal somatosensory regions traditionally thought necessary for discriminative somatic sensations. We hypothesized that if the dpIns subserves the haptic capacity of localization in addition to discrimination, then it should be somatotopically organized. Using functional magnetic resonance imaging to detect activation in the dpIns by graded cooling stimuli applied to the hand and neck, we found unimodal foci arranged in an anteroposterior somatotopographic pattern, consistent with participation of the dpIns in localization as well as discrimination. This gradient is orthogonal to the mediolateral somatotopy of parietal somatosensory regions, which supports the fundamental conceptual differentiation of the interoceptive somatic representation in the dpIns from the parietal exteroceptive representations. These data also support the suggestion that the poststroke central pain syndrome associated with lesions of the dpIns is a thermoregulatory dysfunction. Finally, another focus of strongly graded activation, which we interpret to represent thermoregulatory behavioral motivation elicited by dynamic cooling, was observed in the dorsal medial cortex.temperature; homeostasis; interoception; thermoregulation; functional imaging THERMAL SENSATIONS IN HUMANS (i.e., sensations of cool, warm, cold, and hot) are important for tactile recognition of objects and for homeostatic control of body temperature, functions that are traditionally differentiated as exteroceptive and interoceptive, respectively (28). The exteroceptive aspect of (innocuous and noxious) thermal sensibility has been regarded as a capacity of the somatosensory system, allied with the sense of touch. Specifically, it has been thought that the haptic abilities to discriminate different temperatures and to localize thermal stimuli on the body must involve the somatotopically wellorganized system that represents discriminative cutaneous mechanoreception (23,43). This has been an explicit presumption at least since Weber's analysis of somatic sensation in 1846 (47).However, recent findings indicate that the cortical substrate for discriminative innocuous thermal sensation is not part of the somatosensory cortices but, rather, is located in the insula, which is associated with autonomic control (14). This site is the terminus of a spinothalamocortical pathway, phylogenetically distinct to primates and highly developed in humans, that is an expansion of a homeostatic afferent system representing the physiological condition of the body (16). These new findings fundamentally revise our understanding of the neural representation of feelings from the body (16).To verify and extend these findings, we used functional magnetic resonance imaging (fMRI) to examine thermosensory activation sites in the dorsal posterior insula (dpIns). Our central hypothesis is that if the thermosensory representation in the dpIns partici...

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Section: Discussionmentioning

confidence: 99%

Anteroposterior somatotopy of innocuous cooling activation focus in human dorsal posterior insular cortex

Hua¹,

Strigo²,

Baxter³

et al. 2005

American Journal of Physiology-Regulatory, Integrative and Comp

113

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confidence: 82%

“…In a second study, functional MRI provided evidence on the brain regions involved in body temperature sensation. In this case the amygdala showed significant activation correlated with the sensation of thermal discomfort during exposure of the whole body to cold air (15).No study has specifically investigated the involvement in human thermoregulation of the brainstem, and studies of the brainstem using functional MRI are in their infancy. The application of functional MRI to investigate brainstem responses has been hampered by a number of technical challenges, including magnetic susceptibility and movement-related artifacts.…”

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confidence: 99%

Human medullary responses to cooling and rewarming the skin: A functional MRI study

McAllen

Farrell

Johnson

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

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A fall in skin temperature precipitates a repertoire of thermoregulatory responses that reduce the likelihood of a decrease in core temperature. Studies in animals suggest that medullary raphé neurons are essential for cold-defense, mediating both the cutaneous vasoconstrictor and thermogenic responses to ambient cooling; however, the involvement of raphé neurons in human thermoregulation has not been investigated. This study used functional MRI with an anatomically guided region of interest (ROI) approach to characterize changes in the blood oxygen leveldependent (BOLD) signal within the human medulla of nine normal subjects during non-noxious cooling and rewarming of the skin by a water-perfused body suit. An ROI covering 4.9 ؎ 0.3 mm 2 in the ventral midline of the medulla immediately caudal to the pons (the rostral medullary raphé ) showed an increase in BOLD signal of 3.9% (P < 0.01) during periods of skin cooling, compared with other times. Overall, that signal showed a strong inverse correlation (R ‫؍‬ 0.48, P < 0.001) with skin temperature. A larger ROI covering the internal medullary cross section at the same level (area, 126 ؎ 15 mm 2 ) showed no significant change in mean BOLD signal with cooling (؉0.2%, P > 0.05). These findings demonstrate that human rostral medullary raphé neurons are selectively activated in response to a thermoregulatory challenge and point to the location of thermoregulatory neurons homologous to those of the raphé pallidus nucleus in rodents.functional neuroimaging ͉ raphé ͉ rostral medulla ͉ thermoregulation I n birds and mammals, effective mechanisms have evolved to regulate heat loss and heat production and to maintain body temperature within a limited range. A series of hierarchically organized reflexes act to normalize body temperature: these are driven by thermal detectors of superficial (skin) and deep body temperature (1). Invasive experiments in mammals have established that the dominant detectors of deep body temperature are located in the brain, primarily in the anterior hypothalamus͞ preoptic area, although receptors in the spinal cord and elsewhere also contribute (2). Although the same is presumed to apply to humans, direct evidence is lacking. Recent studies on rats (3-7) and rabbits (8, 9) have now also found that a small brainstem nucleus, the medullary raphé, is a key synaptic relay in the efferent pathways of several heat-conserving mechanisms that are engaged by exposure to cold. Whether these findings on furred animals apply also to humans is unknown.Humans have proved to be an ideal species in which to investigate thermoregulatory mechanisms by noninvasive methods. Such studies have established that, during exposure to a moderately cold environment, skin receptors provide effective feed-forward control of body temperature, such that deep body temperature not only is prevented from falling but often rises (10). Detailed studies have also demonstrated functional interaction between deep body and skin temperatures in the control of thermoregulatory effector m...

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“…However, much progress has been recently achieved as behavioural thermoregulation has become a topic of considerable attention. Examples of this progress include the seminal Wnding that behavioural thermoregulatory responses may not require an intact preoptic area and anterior hypothalamus [PO/AH (Mercer and Simon 2001;Guest et al 2007)] as well as the related discoveries of several cerebral loci involved in behavioural thermoregulation including the insular, cingulate, primary and secondary somatosensory, and orbitofrontal cortex (Craig et al 1994;Davis et al 1998;Becerra et al 1999;Sawamoto et al 2000), the amygdala (Kanosue et al 2002;Verhagen et al 2004), as well as the dorsomedial hypothalamus (Dimicco and Zaretsky 2007).…”

Section: Introductionmentioning

confidence: 99%

Functional architecture of behavioural thermoregulation

Flouris

2010

Eur J Appl Physiol

103

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The human thermoregulatory system relies primarily on behavioural adaptation and secondarily on autonomic and endocrine responses for thermal homeostasis. This is because autonomic and endocrine responses have a limited capacity in preventing hyper/hypothermia in extreme environments. Until recently, the neuroanatomy of behavioural thermoregulation as well as the neuroanatomic substrate of the various thermoregulatory behaviours remained largely unknown. However, this situation has changed in recent years as behavioural thermoregulation has become a topic of considerable attention. The present review evaluates the current knowledge on behavioural thermoregulation in order to summarize the present state-of-the-art and to point towards future research directions. Findings on the fundamental distinction between thermal (dis)comfort and sensation are reviewed showing that the former drives behaviour while the latter initiates autonomic thermoregulation. Moreover, the thermosensitive neurons and thermoeffector functions of behavioural thermoregulation are presented and analysed in a detailed discussion.

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Brain activation during whole body cooling in humans studied with functional magnetic resonance imaging

Cited by 65 publications

References 11 publications

Anteroposterior somatotopy of innocuous cooling activation focus in human dorsal posterior insular cortex

Anteroposterior somatotopy of innocuous cooling activation focus in human dorsal posterior insular cortex

Human medullary responses to cooling and rewarming the skin: A functional MRI study

Functional architecture of behavioural thermoregulation

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