Capsaicin Changes the Pattern of Brain Rhythms in Sleeping Rats

The heat and capsaicin sensor TRPV1 ion channels were originally discovered from sensory neurons in dorsal root ganglia, and later found in many other tissues and organs. However, whether TRPV1 channels are present in brain regions other than hypothalamus has been a subject of debate. Here we addressed this issue with an unbiased functional test, by recording electroencephalogram (EEG) to examine whether capsaicin injection directly into the rat lateral ventricle could alter brain electrical activity. We observed that EEG during the sleep stage could be significantly perturbed by capsaicin, whereas EEG during the awake stage did not show a detectable change. Our results are consistent with TRPV1 expression in selective brain regions whose activities are dominative during the sleep stage.

[1]  B. Szulczyk,et al.  Beneficial Effects of Capsaicin in Disorders of the Central Nervous System , 2022, Molecules.

[2]  B. Szulczyk,et al.  Capsaicin inhibits sodium currents and epileptiform activity in prefrontal cortex pyramidal neurons , 2020, Neurochemistry International.

[3]  Michael C. Chen,et al.  Nigrostriatal and mesolimbic control of sleep–wake behavior in rat , 2019, Brain Structure and Function.

[4]  J. Rinzel,et al.  NREM sleep in the rodent neocortex and hippocampus reflects excitable dynamics , 2019, Nature Communications.

[5]  C. Hsieh,et al.  Targeting TRPV1 to relieve motion sickness symptoms in mice by electroacupuncture and gene deletion , 2018, Scientific Reports.

[6]  A. Adamantidis,et al.  Thalamic dual control of sleep and wakefulness , 2018, Nature Neuroscience.

[7]  S. Chua,et al.  Activation of temperature-sensitive TRPV1-like receptors in ARC POMC neurons reduces food intake , 2018, PLoS biology.

[8]  G. Koob,et al.  Blockade of TRPV1 Inhibits Methamphetamine-induced Rewarding Effects , 2018, Scientific Reports.

[9]  Hyoung‐Chun Kim,et al.  Impairment of opiate‐mediated behaviors by the selective TRPV1 antagonist SB366791 , 2017, Addiction biology.

[10]  S. Schiffmann,et al.  Slow-wave sleep is controlled by a subset of nucleus accumbens core neurons in mice , 2017, Nature Communications.

[11]  Aneesha K. Suresh,et al.  Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity , 2017, Proceedings of the National Academy of Sciences.

[12]  H. Lester,et al.  TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus , 2017, Nature Communications.

[13]  G. Tononi,et al.  Local aspects of sleep and wakefulness , 2017, Current Opinion in Neurobiology.

[14]  M. Boly,et al.  Altered sleep homeostasis correlates with cognitive impairment in patients with focal epilepsy , 2017, Brain : a journal of neurology.

[15]  V. Yarov-Yarovoy,et al.  Rational design and validation of a vanilloid-sensitive TRPV2 ion channel , 2016, Proceedings of the National Academy of Sciences.

[16]  V. Linehan,et al.  Thermosensing mechanisms and their impairment by high-fat diet in orexin neurons , 2016, Neuroscience.

[17]  Sonya M. Hanson,et al.  Engineering vanilloid-sensitivity into the rat TRPV2 channel , 2016, eLife.

[18]  H. Bringmann,et al.  Sleep-active neuron specification and sleep induction require FLP-11 neuropeptides to systemically induce sleep , 2016, eLife.

[19]  G. A. Miller,et al.  Frontal slow-wave activity as a predictor of negative symptoms, cognition and functional capacity in schizophrenia. , 2016, The British journal of psychiatry : the journal of mental science.

[20]  M. Walker,et al.  β-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation , 2015, Nature Neuroscience.

[21]  Paul J. Harrison,et al.  Deletion of Metabotropic Glutamate Receptors 2 and 3 (mGlu2 & mGlu3) in Mice Disrupts Sleep and Wheel-Running Activity, and Increases the Sensitivity of the Circadian System to Light , 2015, PloS one.

[22]  T. Steckler,et al.  Relevance of the metabotropic glutamate receptor (mGluR5) in the regulation of NREM-REM sleep cycle and homeostasis: Evidence from mGluR5 (−/−) mice , 2015, Behavioural Brain Research.

[23]  Hyoung‐Chun Kim,et al.  Transient Receptor Potential Vanilloid Type 1 Channel May Modulate Opioid Reward , 2014, Neuropsychopharmacology.

[24]  S. Schiff,et al.  Rapid Eye Movement Sleep and Hippocampal Theta Oscillations Precede Seizure Onset in the Tetanus Toxin Model of Temporal Lobe Epilepsy , 2014, The Journal of Neuroscience.

[25]  T. Scammell,et al.  Sleep neurobiology from a clinical perspective. , 2011, Sleep.

[26]  D. J. Cavanaugh,et al.  Trpv1 Reporter Mice Reveal Highly Restricted Brain Distribution and Functional Expression in Arteriolar Smooth Muscle Cells , 2011, The Journal of Neuroscience.

[27]  S. Onizuka,et al.  Capsaicin Indirectly Suppresses Voltage-Gated Na+ Currents Through TRPV1 in Rat Dorsal Root Ganglion Neurons , 2011, Anesthesia and analgesia.

[28]  Hyoung‐Chun Kim,et al.  Repeated methamphetamine treatment increases expression of TRPV1 mRNA in the frontal cortex but not in the striatum or hippocampus of mice , 2010, Neuroscience Letters.

[29]  A. A. Romanovsky,et al.  The Transient Receptor Potential Vanilloid-1 Channel in Thermoregulation: A Thermosensor It Is Not , 2009, Pharmacological Reviews.

[30]  Hong-bin Li,et al.  Antistress Effect of TRPV1 Channel on Synaptic Plasticity and Spatial Memory , 2008, Biological Psychiatry.

[31]  Xuesong Cao,et al.  Effects of capsaicin on VGSCs in TRPV1−/− mice , 2007, Brain Research.

[32]  R. Treede,et al.  Capsaicin differentially modulates voltage-activated calcium channel currents in dorsal root ganglion neurones of rats , 2005, Brain Research.

[33]  Mark W. Mahowald,et al.  Insights from studying human sleep disorders , 2005, Nature.

[34]  L. Csiba,et al.  Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. , 2005, Brain research. Molecular brain research.

[35]  Hee-Sup Shin,et al.  Lack of delta waves and sleep disturbances during non-rapid eye movement sleep in mice lacking α1G-subunit of T-type calcium channels , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[36]  John B Davis,et al.  [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution , 2004, Brain Research.

[37]  B. Rockstroh,et al.  Focal temporoparietal slow activity in Alzheimer’s disease revealed by magnetoencephalography , 2002, Biological Psychiatry.

[38]  A I Basbaum,et al.  Impaired nociception and pain sensation in mice lacking the capsaicin receptor. , 2000, Science.

[39]  M. Wilson,et al.  Coordinated Interactions between Hippocampal Ripples and Cortical Spindles during Slow-Wave Sleep , 1998, Neuron.

[40]  C. Epstein,et al.  Primary afferent tachykinins are required to experience moderate to intense pain , 1998, Nature.

[41]  D. Julius,et al.  The capsaicin receptor: a heat-activated ion channel in the pain pathway , 1997, Nature.

[42]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[43]  D. McCormick,et al.  Sleep and arousal: thalamocortical mechanisms. , 1997, Annual review of neuroscience.