Predicting the location of the preoptic and anterior hypothalamic region by visualizing the thermoregulatory center on fMRI in craniopharyngioma using cold and warm stimuli

Hypothalamic nuclei in the preoptic and anterior hypothalamic region (POAH) are critically involved in thermoregulation and neuroendocrine regulation and can be displaced by craniopharyngiomas (CPs). We aimed to locate the POAH by visualizing hypothalamic thermoregulation through task-related functional magnetic resonance imaging (fMRI) to guide hypothalamus protection intraoperatively. Nine adult healthy volunteers (HVs) and thirty-two adult primary CP patients underwent task-related fMRI for POAH localization by warm (60° C) and cold (0° C) cutaneous thermoreceptor stimulation. Approach selection and intraoperative POAH protection were performed based on preoperative POAH localization. In all HVs and patients, significant single positive blood oxygen level-dependent (BOLD) signal changes were located in the POAH. The BOLD activity was significantly greater for cold (P=0.03) and warm (P=0.03) stimuli in patients than in HVs. Gross total resection and near-total resection were achieved in 28 (87.5%) and 4 (12.5%) patients, respectively. New-onset diabetes insipidus and new-onset hypopituitarism occurred in 6 patients (18.8%) and 10 patients (31.3%), respectively. Our findings suggest that cutaneous thermoreceptor stimulation could accurately activate the hypothalamic thermoregulatory center and allow POAH localization through task-related fMRI. Preoperative POAH localization could help neurosurgeons protect hypothalamic function intraoperatively. The CP patients were more sensitive to thermal stimulation.

[1]  Adrian V. Dalca,et al.  Automated segmentation of the hypothalamus and associated subunits in brain MRI , 2020, NeuroImage.

[2]  W. xinsheng,et al.  Approach selection and outcomes of craniopharyngioma resection: a single-institute study , 2020, Neurosurgical Review.

[3]  X. Z. S. Xu,et al.  How to Break a Fever: A Feedback Circuit for Body Temperature Control , 2019, Neuron.

[4]  Michael T. McManus,et al.  Thermoregulation via Temperature-Dependent PGD2 Production in Mouse Preoptic Area , 2019, Neuron.

[5]  E. Nillni,et al.  Endoplasmic Reticulum Stress, the Hypothalamus, and Energy Balance , 2019, Trends in Endocrinology & Metabolism.

[6]  S. Morrison,et al.  Central Mechanisms for Thermoregulation. , 2019, Annual review of physiology.

[7]  Z. Knight,et al.  Regulation of Body Temperature by the Nervous System , 2018, Neuron.

[8]  J. H. Kim,et al.  Endoscopic endonasal approach for craniopharyngioma: the importance of the relationship between pituitary stalk and tumor. , 2017, Journal of neurosurgery.

[9]  C. Thiel,et al.  Hypothalamic tumors impact gray and white matter volumes in fronto-limbic brain areas , 2017, Cortex.

[10]  Wei L. Shen,et al.  Correction for Zhao et al., A hypothalamic circuit that controls body temperature , 2017, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Cuicui Gao,et al.  A hypothalamic circuit that controls body temperature , 2017, Proceedings of the National Academy of Sciences.

[12]  Yen-Chu Lin,et al.  Warm-Sensitive Neurons that Control Body Temperature , 2016, Cell.

[13]  E. Walter,et al.  The neurological and cognitive consequences of hyperthermia , 2016, Critical Care.

[14]  M. Warmuth-Metz,et al.  Survival, hypothalamic obesity, and neuropsychological/psychosocial status after childhood-onset craniopharyngioma: newly reported long-term outcomes. , 2015, Neuro-oncology.

[15]  C. Thiel,et al.  Neuropsychological outcome in patients with childhood craniopharyngioma and hypothalamic involvement. , 2014, The Journal of pediatrics.

[16]  G. Glover.  Overview of functional magnetic resonance imaging. , 2011, Neurosurgery clinics of North America.

[17]  S. Morrison,et al.  A thermosensory pathway mediating heat-defense responses , 2010, Proceedings of the National Academy of Sciences.

[18]  B. Bahuleyan,et al.  Immediate postoperative death due to hypothalamic injury following surgery for craniopharyngioma , 2009, Journal of Clinical Neuroscience.

[19]  Samuel M. McClure,et al.  BOLD Responses Reflecting Dopaminergic Signals in the Human Ventral Tegmental Area , 2008, Science.

[20]  S. Puget,et al.  Craniopharyngioma , 2007, Orphanet journal of rare diseases.

[21]  T. Kaneko,et al.  Medullary dorsal horn neurons providing axons to both the parabrachial nucleus and thalamus , 2006, The Journal of comparative neurology.

[22]  Paul A. M. Smeets,et al.  Functional MRI of human hypothalamic responses following glucose ingestion , 2005, NeuroImage.

[23]  V. Kontopoulos,et al.  Delayed Persistent Hyperthermia after Resection of a Craniopharyngioma , 2004, Pediatric Neurosurgery.

[24]  A. Craig,et al.  Spinothalamic lamina I neurones selectively responsive to cutaneous warming in cats , 2001, The Journal of physiology.

[25]  A. Craig,et al.  Quantitative response characteristics of thermoreceptive and nociceptive lamina I spinothalamic neurons in the cat. , 2001, Journal of neurophysiology.

[26]  G. Johannsson,et al.  The metabolic syndrome and its components in 178 patients treated for craniopharyngioma after 16 years of follow-up. , 2018, European journal of endocrinology.

[27]  S. Rombouts,et al.  The effect of consumption temperature on the homeostatic and hedonic responses to glucose ingestion in the hypothalamus and the reward system. , 2018, The American journal of clinical nutrition.

[28]  G. Johannsson,et al.  Excess morbidity and mortality in patients with craniopharyngioma: a hospital-based retrospective cohort study. , 2018, European journal of endocrinology.

[29]  B. deBoisblanc,et al.  Persistent fever in the ICU. , 2014, Chest.

[30]  S. Morrison,et al.  A thermosensory pathway that controls body temperature , 2008, Nature Neuroscience.