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Serotonergic Neurons in the Caudal Raphe Nuclei Discharge in Association with Activity of Masticatory Muscles

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Serotonergic Neurons in the Caudal Raphe Nuclei Discharge in Association with Activity of Masticatory Muscles SerotonergicBrazilian Journal activity of Medical and masticatory and Biological muscle Research activity (1997) 30: 79-83 79 ISSN 0100-879X Short Communication Serotonergic neurons in the caudal raphe nuclei discharge in association with activity of masticatory muscles L.E. Ribeiro-do-Valle1 1Departamento de Fisiologia e Biofísica, Instituto de Ciências Biomédicas, Universidade de São Paulo, 05508-900 São Paulo, SP, Brasil Abstract Correspondence There is a dense serotonergic projection from nucleus raphe pallidus Key words L.E. Ribeiro-do-Valle and nucleus raphe obscurus to the trigeminal motor nucleus and • Masticatory muscles Departamento de Fisiologia e serotonin exerts a strong facilitatory action on the trigeminal motoneu- • Serotonergic neurons Biofísica rons. Some serotonergic neurons in these caudal raphe nuclei increase • Caudal raphe nuclei Instituto de Ciências Biomédicas their discharge during feeding. The objective of the present study was • Feeding behavior Universidade de São Paulo • Grooming behavior 05508-900 São Paulo, SP to investigate the possibility that the activity of these serotonergic Brasil neurons is related to activity of masticatory muscles. Cats were E-mail: [email protected] implanted with microelectrodes and gross electrodes. Caudal raphe single neuron activity, electrocorticographic activity, and splenius, Research supported by FAPESP and digastric and masseter electromyographic activities were recorded CNPq. during active behaviors (feeding and grooming), during quiet waking and during sleep. Seven presumed serotonergic neurons were identi- fied. These neurons showed a long duration action potential (>2.0 Received June 4, 1996 msec), and discharged slowly (2-7 Hz) and very regularly (interspike Accepted November 11, 1996 interval coefficient of variation <0.3) during quiet waking. The activ- ity of these neurons decreased remarkably during fast wave sleep (78- 100%). Six of these neurons showed tonic changes in their activity positively related to digastric and/or masseter muscles activity but not to splenius muscle activity during waking. These data are consistent with the hypothesis that serotonergic neurons in the caudal raphe nuclei play an important role in the control of jaw movements. The trigeminal motor nucleus receives a the control of jaw muscles activity. dense serotonergic projection (1,2) which It is well known that the activity of the originates from nucleus raphe pallidus, serotonergic neurons in the raphe nuclei is nucleus raphe obscurus and, to a lesser ex- related to the level of arousal of the organism tent, from nucleus raphe dorsalis (3,4). Sero- (for a review, see Ref. 8). Thus, the tonic tonergic fibers terminate in close proximity serotonergic influence on the trigeminal to the cell body and proximal processes of motoneurons during waking may contribute trigeminal motoneurons (1,5). Serotonin was to maintaining jaw position and facilitating shown to strongly facilitate trigeminal moto- jaw movements during feeding, grooming, neurons (6,7). These findings suggest an im- and defense/aggression behaviors. portant role for the serotonergic system in It has been shown that some serotonergic Braz J Med Biol Res 30(1) 1997 80 L.E. Ribeiro-do-Valle et al. neurons in nucleus raphe dorsalis selectively by moving the microdrive screw 1/4 turn. increase their activity during feeding and When a recordable spike was found the ani- grooming behaviors (9,10). Many serotoner- mals were further tested. Neuronal activity gic neurons in nucleus raphe pallidus and as well as the EEG and 3 EMG were re- nucleus raphe obscurus behave similarly (11). corded during quiet waking, slow wave sleep These results raise the interesting possibility and fast wave sleep, and while the subject that there may be additional changes in the was exhibiting spontaneous behaviors such serotonergic influence on the trigeminal mo- as feeding and grooming. All signals were toneurons associated with the activation of recorded on paper and on videotape. Sponta- these motoneurons by central mechanisms neous behaviors of the subjects and neuronal during behaviors that involve oral move- activity were recorded together on another ments. In the present study we investigated videotape. this hypothesis. After advancing the microelectrodes Adult cats of either sex were used. Hous- about 5 mm into the brainstem, the animals ing conditions of the animals and the exper- were sacrificed and their hindbrain was pro- imental protocol were reviewed and approved cessed histologically to locate the recorded by the Comissão de Fiscalização de Pesquisa neurons (for details see Ref. 13). com Animais (COFIPA) of São Paulo City. The data were treated as follows: 1) Neu- For single neuron recording the animals were ronal action potential duration was meas- stereotaxically implanted with a microdrive ured. 2) Neuronal discharge was evaluated consisting of two inner cannulas that could during 5 min of quiet waking, 5 min of slow be moved along outer guide cannulas by wave sleep and 5 min of fast wave sleep. turning a small screw. Two bundles of 6 State-dependent changes in cell activity were microelectrodes (32- and 64-µm diameter determined by comparing firing rate across Formvar-insulated nichrome wires) were the wake-sleep cycle using the Friedman lowered through the inner cannulas to the two-way test and Wilcoxon signed rank test. coordinates AP -11.6 and -12.6, LM ±0.0 Regularity of cell discharge during quiet and DV -0.2 of the Snider and Niemer (12) waking was determined by calculating the atlas of the cat brain and then glued to the top interspike interval coefficient of variation of these cannulas. Gross electrodes were (standard deviation/mean). 3) Neuronal dis- implanted into the digastric, masseter and charge and muscle activity were evaluated splenius muscles (the digastric and masseter during 20 sec of quiet waking, 60 sec of muscles are the major jaw-opening and jaw- drinking milk, 20 sec of licking lips and 20 closing muscles, respectively) and threaded sec of licking forelimbs/washing face: a) A into the parietal, frontal, temporal and possible tight phasic coupling between retroorbital bones to record muscular activ- muscle activity and neuron activity was ex- ity (EMG), cortical activity (EEG) and eye amined by averaging full-wave rectified movements (EOG). The microdrive and elec- muscle activity 25 msec before and 25 msec trode implantation procedures are described after each spike across all the spikes, for in detail by Heym et al. (13). drinking milk (this procedure is known as Testing was initiated after a recovery spike-triggered waveform averaging). The period of 2 weeks following surgery. All criterion for considering the existence of microelectrodes were screened 2 to 3 times a coupling was a post-spike muscle activity day for the presence of stable, isolated single- change with respect to mean pre-spike muscle unit activity (signal to noise ratio >3). In the activity exceeding by at least 50% the maxi- absence of this activity the microelectrodes mum pre-spike muscle activity change with were advanced in small steps (about 80 µm) respect to mean pre-spike muscle activity Braz J Med Biol Res 30(1) 1997 Serotonergic activity and masticatory muscle activity 81 over a period of 1 msec. b) A possible gross quiet waking, drinking milk, licking lips and tonic relationship between neuronal activity licking forelimbs/washing face. The dis- and muscular activity was determined by charge of these neurons tended to increase correlating the number of spikes per two 10- from quiet waking to licking lips to licking sec epochs of quiet waking, drinking milk, forelimbs/washing face and drinking milk. licking lips and licking forelimbs/washing Muscle activity changed considerably from face with the corresponding integrated mus- one behavior to another. Digastric muscle cular voltages. c) A possible fine tonic rela- activity tended to increase from quiet wak- tionship between neuronal activity and ing to licking forelimbs/washing face to lick- muscular activity was examined by correlat- ing lips and drinking milk; masseter muscle ing the number of spikes per six 10-sec epochs activity tended to increase from quiet wak- of drinking milk with the corresponding in- ing to licking lips to drinking milk and lick- tegrated muscular voltages. (For both b) and c) ing forelimbs/washing face; and splenius the Spearman rank correlation test was used.) muscle activity tended to increase from quiet Seven neurons that showed a long-dura- waking to drinking milk to licking lips and tion action potential (>2.0 msec) and slow (2 licking forelimbs/washing face. Five of the to 7 Hz) and very regular (interspike interval neurons changed their firing rate in relation coefficient of variation <0.3) discharge dur- to muscle activity. For 1 neuron the firing ing quiet waking were recorded in two ani- rate was related to digastric muscle activity mals. All of them systematically changed (rS = 0.77; P = 0.04). For 2 other neurons the their activity across the wake-sleep cycle. firing rate was related to masseter muscle The firing rate decreased from quiet waking activity (rS = 0.79 and rS = 0.79; P = 0.04). to slow wave sleep (the respective means ± For the last 2 neurons the firing rate was SEM for six of these neurons were: 3.86 ± related to digastric (rS = 0.90 and rS = 0.90; P 0.73 and 3.15 ± 0.76 Hz; P = 0.02) and from = 0.02) and masseter (rS = 0.83 and rS = 0.90; slow wave sleep to fast wave sleep (the P = 0.03 and P = 0.02, respectively) muscles respective means ± SEM for the same six activity (Figure 1). neurons were: 3.15 ± 0.76 and 0.24 ± 0.17 Of the 6 neurons that could be evaluated Hz; P = 0.02). One of these neurons was during a 60-sec period of drinking milk only 2 located in the dorsal third, 2 in the middle discharged in association with muscle activity.
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