Capsaicin Changes the Pattern of Brain Rhythms in Sleeping Rats
Abstract
:1. Introduction
2. Results
2.1. Capsaicin and Injection Effectiveness Tests
2.2. Recording Changes in EEGs upon Brain Injection of Capsaicin
2.3. Capsaicin Produced a Significant Change in the Pattern of Brain Rhythms in the Sleeping Stage
2.4. Capsaicin Did Not Produce Detectable Changes in the Pattern of Brain Rhythms in the Awake Stage
3. Discussion
4. Materials and Methods
4.1. Chemicals
4.2. Animals
4.3. Control Experiments
4.4. Implant Procedure
4.5. EEG Recording and Analysis
4.6. Statistical Analysis
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Sample Availability
Abbreviations
TRPV1 | Transient receptor potential cation channel, subfamily V, member 1 |
EEG | Electroencephalogram |
References
- Caterina, M.J.; Schumacher, M.A.; Tominaga, M.; Rosen, T.A.; Levine, J.D.; Julius, D. The capsaicin receptor: A heat-activated ion channel in the pain pathway. Nature 1997, 389, 816–824. [Google Scholar] [CrossRef] [PubMed]
- Yang, F.; Vu, S.; Yarov-Yarovoy, V.; Zheng, J. Rational design and validation of a vanilloid-sensitive TRPV2 ion channel. Proc. Natl. Acad. Sci. USA 2016, 113, E3657–E3666. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, F.; Hanson, S.M.; Jara-Oseguera, A.; Krepkiy, D.; Bae, C.; Pearce, L.V.; Blumberg, P.M.; Newstead, S.; Swartz, K.J. Engineering vanilloid-sensitivity into the rat TRPV2 channel. Elife 2016, 5, e16409. [Google Scholar] [CrossRef] [PubMed]
- Caterina, M.J.; Leffler, A.; Malmberg, A.B.; Martin, W.J.; Trafton, J.; Petersen-Zeitz, K.R.; Koltzenburg, M.; Basbaum, A.I.; Julius, D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288, 306–313. [Google Scholar] [CrossRef] [PubMed]
- Pasierski, M.; Szulczyk, B. Beneficial Effects of Capsaicin in Disorders of the Central Nervous System. Molecules 2022, 27, 2484. [Google Scholar] [CrossRef]
- Pasierski, M.; Szulczyk, B. Capsaicin inhibits sodium currents and epileptiform activity in prefrontal cortex pyramidal neurons. Neurochem. Int. 2020, 135, 104709. [Google Scholar] [CrossRef]
- Onizuka, S.; Yonaha, T.; Tamura, R.; Hosokawa, N.; Kawasaki, Y.; Kashiwada, M.; Shirasaka, T.; Tsuneyoshi, I. Capsaicin indirectly suppresses voltage-gated Na+ currents through TRPV1 in rat dorsal root ganglion neurons. Anesth. Analg. 2011, 112, 703–709. [Google Scholar] [CrossRef]
- Hagenacker, T.; Splettstoesser, F.; Greffrath, W.; Treede, R.D.; Büsselberg, D. Capsaicin differentially modulates voltage-activated calcium channel currents in dorsal root ganglion neurones of rats. Brain Res. 2005, 1062, 74–85. [Google Scholar] [CrossRef]
- Turek, M.; Besseling, J.; Spies, J.P.; Konig, S.; Bringmann, H. Sleep-active neuron specification and sleep induction require FLP-11 neuropeptides to systemically induce sleep. Elife 2016, 5, e12499. [Google Scholar] [CrossRef]
- Siclari, F.; Tononi, G. Local aspects of sleep and wakefulness. Curr. Opin. Neurobiol. 2017, 44, 222–227. [Google Scholar] [CrossRef]
- Mahowald, M.W.; Schenck, C.H. Insights from studying human sleep disorders. Nature 2005, 437, 1279–1285. [Google Scholar] [CrossRef] [PubMed]
- Sedigh-Sarvestani, M.; Thuku, G.I.; Sunderam, S.; Parkar, A.; Weinstein, S.L.; Schiff, S.J.; Gluckman, B.J. Rapid eye movement sleep and hippocampal theta oscillations precede seizure onset in the tetanus toxin model of temporal lobe epilepsy. J. Neurosci. 2014, 34, 1105–1114. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, J.; Kim, D.; Shin, H.S. Lack of delta waves and sleep disturbances during non-rapid eye movement sleep in mice lacking alpha1G-subunit of T-type calcium channels. Proc. Natl. Acad. Sci. USA 2004, 101, 18195–18199. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ahnaou, A.; Raeymaekers, L.; Steckler, T.; Drinkenbrug, W.H. Relevance of the metabotropic glutamate receptor (mGluR5) in the regulation of NREM-REM sleep cycle and homeostasis: Evidence from mGluR5 (−/−) mice. Behav. Brain Res. 2015, 282, 218–226. [Google Scholar] [CrossRef]
- Pritchett, D.; Jagannath, A.; Brown, L.A.; Tam, S.K.; Hasan, S.; Gatti, S.; Harrison, P.J.; Bannerman, D.M.; Foster, R.G.; Peirson, S.N. 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. PLoS ONE 2015, 10, e0125523. [Google Scholar] [CrossRef] [Green Version]
- Boly, M.; Jones, B.; Findlay, G.; Plumley, E.; Mensen, A.; Hermann, B.; Tononi, G.; Maganti, R. Altered sleep homeostasis correlates with cognitive impairment in patients with focal epilepsy. Brain 2017, 140, 1026–1040. [Google Scholar] [CrossRef] [Green Version]
- Chen, Y.H.; Stone-Howell, B.; Edgar, J.C.; Huang, M.; Wootton, C.; Hunter, M.A.; Lu, B.Y.; Sadek, J.R.; Miller, G.A.; Canive, J.M. Frontal slow-wave activity as a predictor of negative symptoms, cognition and functional capacity in schizophrenia. Br. J. Psychiatry 2016, 208, 160–167. [Google Scholar] [CrossRef] [Green Version]
- Fernandez, A.; Maestu, F.; Amo, C.; Gil, P.; Fehr, T.; Wienbruch, C.; Rockstroh, B.; Elbert, T.; Ortiz, T. Focal temporoparietal slow activity in Alzheimer’s disease revealed by magnetoencephalography. Biol. Psychiatry 2002, 52, 764–770. [Google Scholar] [CrossRef] [Green Version]
- Jeong, J.H.; Lee, D.K.; Liu, S.M.; Chua, S.C., Jr.; Schwartz, G.J.; Jo, Y.H. Activation of temperature-sensitive TRPV1-like receptors in ARC POMC neurons reduces food intake. PLoS Biol. 2018, 16, e2004399. [Google Scholar] [CrossRef] [Green Version]
- Cavanaugh, D.J.; Chesler, A.T.; Jackson, A.C.; Sigal, Y.M.; Yamanaka, H.; Grant, R.; O’Donnell, D.; Nicoll, R.A.; Shah, N.M.; Julius, D.; et al. Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J. Neurosci. 2011, 31, 5067–5077. [Google Scholar] [CrossRef] [Green Version]
- Belanger-Willoughby, N.; Linehan, V.; Hirasawa, M. Thermosensing mechanisms and their impairment by high-fat diet in orexin neurons. Neuroscience 2016, 324, 82–91. [Google Scholar] [CrossRef] [PubMed]
- Romanovsky, A.A.; Almeida, M.C.; Garami, A.; Steiner, A.A.; Norman, M.H.; Morrison, S.F.; Nakamura, K.; Burmeister, J.J.; Nucci, T.B. The transient receptor potential vanilloid-1 channel in thermoregulation: A thermosensor it is not. Pharmacol. Rev. 2009, 61, 228–261. [Google Scholar] [CrossRef] [PubMed]
- Tian, Y.H.; Ma, S.X.; Lee, K.W.; Wee, S.; Koob, G.F.; Lee, S.Y.; Jang, C.G. Blockade of TRPV1 Inhibits Methamphetamine-induced Rewarding Effects. Sci. Rep. 2018, 8, 882. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ma, S.X.; Kwon, S.H.; Seo, J.Y.; Hwang, J.Y.; Hong, S.I.; Kim, H.C.; Lee, S.Y.; Jang, C.G. Impairment of opiate-mediated behaviors by the selective TRPV1 antagonist SB366791. Addict. Biol. 2017, 22, 1817–1828. [Google Scholar] [CrossRef]
- Nguyen, T.L.; Kwon, S.H.; Hong, S.I.; Ma, S.X.; Jung, Y.H.; Hwang, J.Y.; Kim, H.C.; Lee, S.Y.; Jang, C.G. Transient receptor potential vanilloid type 1 channel may modulate opioid reward. Neuropsychopharmacology 2014, 39, 2414–2422. [Google Scholar] [CrossRef] [Green Version]
- Oishi, Y.; Xu, Q.; Wang, L.; Zhang, B.J.; Takahashi, K.; Takata, Y.; Luo, Y.J.; Cherasse, Y.; Schiffmann, S.N.; de Kerchove d’Exaerde, A.; et al. Slow-wave sleep is controlled by a subset of nucleus accumbens core neurons in mice. Nat. Commun. 2017, 8, 734. [Google Scholar] [CrossRef] [Green Version]
- Qiu, M.H.; Zhong, Z.G.; Chen, M.C.; Lu, J. Nigrostriatal and mesolimbic control of sleep-wake behavior in rat. Brain Struct. Funct. 2019, 224, 2525–2535. [Google Scholar] [CrossRef]
- Toth, A.; Boczan, J.; Kedei, N.; Lizanecz, E.; Bagi, Z.; Papp, Z.; Edes, I.; Csiba, L.; Blumberg, P.M. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res. Mol. Brain Res. 2005, 135, 162–168. [Google Scholar] [CrossRef]
- Hurtado-Zavala, J.I.; Ramachandran, B.; Ahmed, S.; Halder, R.; Bolleyer, C.; Awasthi, A.; Stahlberg, M.A.; Wagener, R.J.; Anderson, K.; Drenan, R.M.; et al. TRPV1 regulates excitatory innervation of OLM neurons in the hippocampus. Nat. Commun. 2017, 8, 15878. [Google Scholar] [CrossRef] [Green Version]
- Li, H.B.; Mao, R.R.; Zhang, J.C.; Yang, Y.; Cao, J.; Xu, L. Antistress effect of TRPV1 channel on synaptic plasticity and spatial memory. Biol. Psychiatry 2008, 64, 286–292. [Google Scholar] [CrossRef]
- Tian, Y.H.; Lee, S.Y.; Kim, H.C.; Jang, C.G. Repeated methamphetamine treatment increases expression of TRPV1 mRNA in the frontal cortex but not in the striatum or hippocampus of mice. Neurosci. Lett. 2010, 472, 61–64. [Google Scholar] [CrossRef] [PubMed]
- Mander, B.A.; Marks, S.M.; Vogel, J.W.; Rao, V.; Lu, B.; Saletin, J.M.; Ancoli-Israel, S.; Jagust, W.J.; Walker, M.P. beta-amyloid disrupts human NREM slow waves and related hippocampus-dependent memory consolidation. Nat. Neurosci. 2015, 18, 1051–1057. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Levenstein, D.; Buzsaki, G.; Rinzel, J. NREM sleep in the rodent neocortex and hippocampus reflects excitable dynamics. Nat. Commun. 2019, 10, 2478. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Siapas, A.G.; Wilson, M.A. Coordinated interactions between hippocampal ripples and cortical spindles during slow-wave sleep. Neuron 1998, 21, 1123–1128. [Google Scholar] [CrossRef] [Green Version]
- Espana, R.A.; Scammell, T.E. Sleep neurobiology from a clinical perspective. Sleep 2011, 34, 845–858. [Google Scholar] [CrossRef]
- Durkin, J.; Suresh, A.K.; Colbath, J.; Broussard, C.; Wu, J.; Zochowski, M.; Aton, S.J. Cortically coordinated NREM thalamocortical oscillations play an essential, instructive role in visual system plasticity. Proc. Natl. Acad. Sci. USA 2017, 114, 10485–10490. [Google Scholar] [CrossRef] [Green Version]
- Gent, T.C.; Bandarabadi, M.; Herrera, C.G.; Adamantidis, A.R. Thalamic dual control of sleep and wakefulness. Nat. Neurosci. 2018, 21, 974–984. [Google Scholar] [CrossRef]
- McCormick, D.A.; Bal, T. Sleep and arousal: Thalamocortical mechanisms. Annu. Rev. Neurosci. 1997, 20, 185–215. [Google Scholar] [CrossRef] [Green Version]
- Steriade, M.; McCormick, D.A.; Sejnowski, T.J. Thalamocortical oscillations in the sleeping and aroused brain. Science 1993, 262, 679–685. [Google Scholar] [CrossRef]
- Inprasit, C.; Lin, Y.W.; Huang, C.P.; Wu, S.Y.; Hsieh, C.L. Targeting TRPV1 to relieve motion sickness symptoms in mice by electroacupuncture and gene deletion. Sci. Rep. 2018, 8, 10365. [Google Scholar] [CrossRef] [Green Version]
- Roberts, J.C.; Davis, J.B.; Benham, C.D. [3H]Resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res. 2004, 995, 176–183. [Google Scholar] [CrossRef] [PubMed]
- Cao, X.; Cao, X.; Xie, H.; Yang, R.; Lei, G.; Li, F.; Li, A.; Liu, C.; Liu, L. Effects of capsaicin on VGSCs in TRPV1-/- mice. Brain Res. 2007, 1163, 33–43. [Google Scholar] [CrossRef] [PubMed]
- Cao, Y.Q.; Mantyh, P.W.; Carlson, E.J.; Gillespie, A.M.; Epstein, C.J.; Basbaum, A.I. Primary afferent tachykinins are required to experience moderate to intense pain. Nature 1998, 392, 390–394. [Google Scholar] [CrossRef] [PubMed]
Delta Wave | Theta Wave | Alpha Wave | Beta Wave | |
---|---|---|---|---|
vehicle | 35.94 ± 2.85% | 7.07 ± 0.70% | 2.99 ± 0.59% | 7.30 ± 1.29% |
23 μg/2 μL capsaicin | 41.14 ± 1.56% | 5.39 ± 0.19% | 2.02 ± 0.33% | 4.47 ± 0.45% |
70 μg/2 μL capsaicin | 24.56 ± 1.09% $ | 10.21 ± 0.64% # | 5.60 ± 0.42% & | 11.74 ± 0.07% |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Liu, L.; Tian, Y. Capsaicin Changes the Pattern of Brain Rhythms in Sleeping Rats. Molecules 2023, 28, 4736. https://doi.org/10.3390/molecules28124736
Liu L, Tian Y. Capsaicin Changes the Pattern of Brain Rhythms in Sleeping Rats. Molecules. 2023; 28(12):4736. https://doi.org/10.3390/molecules28124736
Chicago/Turabian StyleLiu, Lei, and Yuhua Tian. 2023. "Capsaicin Changes the Pattern of Brain Rhythms in Sleeping Rats" Molecules 28, no. 12: 4736. https://doi.org/10.3390/molecules28124736