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Altered Activity in the Nucleus Raphe Magnus Underlies Cortical Hyperexcitability and Facilitates Trigeminal Nociception in a Ra

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Altered Activity in the Nucleus Raphe Magnus Underlies Cortical Hyperexcitability and Facilitates Trigeminal Nociception in a Ra Potewiratnanond et al. BMC Neurosci (2019) 20:54 https://doi.org/10.1186/s12868-019-0536-2 BMC Neuroscience RESEARCH ARTICLE Open Access Altered activity in the nucleus raphe magnus underlies cortical hyperexcitability and facilitates trigeminal nociception in a rat model of medication overuse headache Prangtip Potewiratnanond1, Supang Maneesri le Grand2, Anan Srikiatkhachorn3 and Weera Supronsinchai4* Abstract Background: The pathogenesis of medication overuse headache (MOH) involves hyperexcitability of cortical and trigeminal neurons. Derangement of the brainstem modulating system, especially raphe nuclei may contribute to this hyperexcitability. The present study aimed to investigate the involvement of the nucleus raphe magnus (NRM) in the development of cortical and trigeminal hyperexcitability in a rat model of MOH. Results: Chronic treatment with acetaminophen increased the frequency of cortical spreading depression (CSD) and the number of c-Fos-immunoreactive (Fos-IR) neurons in the trigeminal nucleus caudalis (TNC). In the control group, muscimol microinjected into the NRM increased signifcantly the frequency of CSD-evoked direct current shift and Fos-IR neurons in the TNC. This facilitating efect was not found in rats with chronic acetaminophen exposure. In a model of migraine induced by intravenous systemic infusion of nitroglycerin (NTG), rats with chronic exposure to acetaminophen exhibited signifcantly more frequent neuronal fring in the TNC and greater Fos-IR than those with- out the acetaminophen treatment. Muscimol microinjection increased neuronal fring in the TNC in control rats, but not in acetaminophen-treated rats. The number of Fos-IR cells in TNC was not changed signifcantly. Conclusion: Chronic exposure to acetaminophen alters the function of the NRM contributing to cortical hyperexcit- ability and facilitating trigeminal nociception. Keywords: Acetaminophen, Cortical spreading depression, Extracellular recording, Nitroglycerin, Nucleus raphe magnus, Paracetamol, Trigeminal nucleus caudalis Background or more days/month) in a patient with pre-existing pri- Overconsumption of medication to abort headaches, mary headaches and develops as a consequence of regu- either migraine specifc agents, or narcotic or non- lar overuse (10 to 15 or more days/month, depending on narcotic analgesics, is a known factor for deteriorating medication) of acute or symptomatic headache medica- headache symptoms in patients with primary headaches, tion for more than 3 months. It usually, but not invari- especially migraine and tension-type headache. Tis ably, resolves after overuse is stopped [1]. Tis condition overconsumption contributes to the development of a is one of the most common chronic headaches with a syndrome known clinically as “medication overuse head- prevalence of 1–2% worldwide [2]. ache” (MOH). MOH refers to a frequent headache (15 Te mechanism by which abortive medication worsens clinical headache remains unclear. One hypothesis is neu- ronal hyperexcitability [3]. Preclinical studies show that *Correspondence: [email protected] 4 Department of Physiology, Faculty of Dentistry, Chulalongkorn chronic analgesic drug exposure can increase neuronal University, Bangkok, Thailand excitability in the cerebral cortex and trigeminal nocicep- Full list of author information is available at the end of the article tive system. For instance, expanded cutaneous receptive © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Potewiratnanond et al. BMC Neurosci (2019) 20:54 Page 2 of 10 felds and reduced thresholds to painful stimuli were allowed unrestrained access to standard laboratory food demonstrated in rats with sustained morphine exposure and tap water. To limit the efect of nonspecifc stress, all [4]. Persistent administration of a triptan to rats elicited rats were acclimatized to daily handling for at least 3 days periorbital cutaneous allodynia [5]. An increase in fre- before experiments. quency of cortical spreading depression (CSD) and num- ber of CSD-evoked c-Fos-immunoreactive (Fos-IR) cells Drugs and treatments in the trigeminal nucleus caudalis (TNC) was demon- Acetaminophen (paracetamol) in solution (300 mg/2 mL) strated in rats receiving acetaminophen or dihydroergot- was purchased from T.P. Drug Laboratories (Bangkok, amine [3, 6]. Te hypothesis of cortical hyperexcitability Tailand). Te acetaminophen dose used in present is supported by clinical evidence. In patients with MOH, experiments was 200 mg/kg as consistent with previous the amplitude of pain-related cortical potentials (PREP) studies [3, 6, 7, 10]. Normal saline was administered to evoked by electrical sensory stimulus on the forehead or rats in a vehicle-treated control group. Te volume of a limb were greater than they were in a control group. all drug injections was calculated according to standard Te facilitation of both trigeminal and somatic PREP in criteria (intraperitoneally 10 mL/kg). Doses of acetami- those patients became normalized after drug withdrawal nophen were chosen based on the presence of efcacy [7]. Patients with MOH also had larger amplitude soma- without serious adverse efects. Intraperitoneal injec- tosensory evoked potentials (SEP) than nonheadache tions of the acetaminophen or saline vehicle control were control patients, and lacked SEP habituation [8]. administered at a similar time of day (8:00 to 9:00 a.m.). Derangement of serotonergic systems in the raphe Muscimol was purchased from Calbiochem (Merck). nuclei may contribute to this neuronal hyperexcitabil- Nitroglycerin was purchased from Pharmaland (Bang- ity. Preclinical studies showed that rats with depleted kok, Tailand). Each subgroup comprised 6–8 rats. serotonin levels exhibited similar features to rats with chronic exposure to medication. Tese features include Study design increased CSD susceptibility, facilitated trigeminal noci- Studies were divided into two experiments. Te frst was ception, and upregulated pronociceptive messengers, aimed at determining the modulating efect of NRM on such as nitric oxide [9, 10]. Some clinical observations CSD, CSD-induced cortical hyperemia, and CSD-evoked indicate that the serotonin system is altered in patients Fos-IR in the TNC. In this experiment, rats were divided with chronic headache both with and without medication into two groups, an acetaminophen-treated group and a overuse. For example, D’Andrea et al. [11] showed that vehicle-treated control group. Intraperitoneal injections the plasma level of tryptophan was signifcantly lower in were made on 30 consecutive days. On day 31, rats were patients with chronic migraine and chronic tension-type prepared to record electrocortical activity and cortical headache. Lower levels of platelet serotonin and upregu- blood fow. CSD was elicited by applying solid KCl to the lation of pronociceptive 5-HT2A serotonin receptors was exposed cortex. CSD and CSD-evoked changes in CBF found in patients with MOH [12, 13]. recorded during the frst 30 min after applying KCl were Te primary objective of the present study was to used as baseline data. Muscimol (10 nM, 0.2 µL) or 0.9% investigate the involvement of the nucleus raphe mag- NaCl (0.2 µL), both of which contained Pontamine Sky nus (NRM) in the pathogenesis of MOH. We used two Blue to mark the microinjection site, was microinjected animal models of migraine, efected by KCl-evoked CSD into the NRM 30 min after eliciting a CSD, and electro- and intravenous systemic nitroglycerin (NTG) infusion. cortical activity and cortical blood fow were recorded Serotonergic function was inhibited by direct microinjec- for a further 90 min. After completing the recordings, the tion of the GABA A agonist muscimol into the NRM. We brainstem was removed for immunohistochemistry to measured trigeminal neuron activity by recording extra- determine the expression of c-Fos. cellular activity and counting the number of Fos-IR cells A second experiment was designed to study the efect neurons in the TNC. of inhibiting the NRM on NTG-evoked trigeminal nocic- eption. Rats were divided into an acetaminophen-treated Methods group and a vehicle-treated control group (n = 15 or 16 Animals each respectively). Te drug administration protocol was Adult male Wistar rats weighing 180–200 g were the same as for the CSD experiment. On day 31, rats were obtained from the National Laboratory Animal Center, prepared for extracellular recording of neurons in the Mahidol University. Te rats were housed in cages with TNC. Te spontaneous activity of neurons in the TNC stainless-steel bases covered in wood shavings (4–5 was recorded for 10 min as a baseline and then NTG was animals per cage), at an ambient room temperature infused intravenously (0.5 mg/kg, infusion rate 0.5 mL/h). of 25–30 °C under a 12 h photoperiod. Te rats were One hour after the infusion, muscimol or 0.9% NaCl Potewiratnanond et al. BMC Neurosci (2019) 20:54 Page 3 of 10 (n = 7 or 8 per subgroup) was microinjected into NRM. inserted into the NRM. Te
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