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Excitatory and Inhibitory Innervation of the Mouse Orofacial Motor Nuclei: a Stereological Study

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Excitatory and Inhibitory Innervation of the Mouse Orofacial Motor Nuclei: a Stereological Study RESEARCH ARTICLE Excitatory and Inhibitory Innervation of the Mouse Orofacial Motor Nuclei: A Stereological Study Macarena Faunes,1,2 Alejandro Onate-Ponce,~ 1,2 Sara Fernandez-Collemann,1,2 and Pablo Henny1,2* 1Laboratorio de Neuroanatomıa, Departamento de Anatomıa Normal, Escuela de Medicina, Pontificia Universidad Catolica de Chile, Santiago, Chile 2Centro Interdisciplinario de Neurociencias, Pontificia Universidad Catolica de Chile, Santiago, Chile ABSTRACT 3,000, 600, and 1,700 cells, respectively. Neurons in the trigeminal (Mo5), facial (Mo7), ambiguus VGluT11,VGluT21, and VIAAT1 varicosities respec- (Amb), and hypoglossal (Mo12) motor nuclei innervate tively represent: 28%, 41%, and 31% in Mo5; 2%, 49%, jaw, facial, pharynx/larynx/esophagus, and tongue and 49% in Mo7; 12%, 42%, and 46% in Amb; and 4%, muscles, respectively. They are essential for movements 54%, and 42% in Mo12. The Mo5 jaw-closing subdivision subserving feeding, exploration of the environment, and shows the highest VGluT11 innervation. Noticeably, the social communication. These neurons are largely con- VGluT21 and VIAAT1 varicosity density in Mo7 is 5-fold trolled by sensory afferents and premotor neurons of the higher than in Mo5 and 10-fold higher than in Amb and reticular formation, where central pattern generator cir- Mo12. The high density of terminals in Mo7 likely cuits controlling orofacial movements are located. To reflects the convergence and integration of numerous provide a description of the orofacial nuclei of the adult inputs to motoneurons subserving the wide range of mouse and to ascertain the influence of excitatory and complex behaviors to which this nucleus contributes. inhibitory afferents upon them, we used stereology to Also, somatic versus neuropil location of varicosities sug- estimate the number of motoneurons as well as of vari- gests that most of these afferents are integrated in the cosities immunopositive for glutamate (VGluT11, dendritic trees of Mo7 neurons. J. Comp. Neurol. VGluT21) and GABA/glycine (known as VIAAT1 or 524:738–758, 2016. VGAT1) vesicular transporters in the Mo5, Mo7, Amb, and Mo12. Mo5, Mo7, Amb, and Mo12 contain 1,000, VC 2015 Wiley Periodicals, Inc. INDEXING TERMS: AB_1966444; AB_2079751; AB_2254574; AB_2315551; AB_2340593; AB_2340396; facial nucleus; hypoglossal nucleus; mouse brainstem; nucleus ambiguus; trigeminal motor nucleus; vesicular transporters; VGAT; VGluT1; VGluT2; VIAAT Mammalian orofacial muscles are involved in vital involved in the rhythmic exploratory behavior-related non-locomotive behaviors including suckling, mastica- movements whisking and sniffing (Deschenes^ et al., tion, swallowing, whisking, facial expression, and the 2012), ear wiggling, and other movements such as production of vocalizations, among others. In humans, blinking. These various patterns of activity are con- they are also involved in the production of speech. Jaw, trolled by brainstem premotor networks and influenced facial, pharynx/larynx/esophagus, and tongue muscles are innervated by motoneurons located in the trigeminal (Mo5), facial (Mo7), ambiguus (Amb), and hypoglossal Grant sponsor: FONDECYT; Grant number: 11100433; Grant sponsor: Anillo; Grant number: ACT-1109, CONICYT, Chile. (Mo12) brainstem motor nuclei, respectively. Current address for Macarena Faunes: Sensory and Motor Systems Group, Department of Anatomy with Radiology, Faculty of Medical and Feeding-related movements, such as mastication, Health Sciences, University of Auckland, Private Bag 92019, Grafton, suckling and licking, involve the rhythmic activity of 1023, Auckland, New Zealand. Mo5 in coordination with Mo7 and Mo12 (Nakamura *CORRESPONDENCE TO: Pablo Henny, Laboratorio de Neuroanatomıa, Departamento de Anatomıa Normal, Escuela de Medicina, Pontificia and Katakura, 1995; Travers et al., 1997). These move- Universidad Catolica de Chile. Casa central, Alameda 340, Comuna de ments are often followed by swallowing, where Amb Santiago, Santiago, Chile. E-mail: [email protected] motoneurons take part as well (Jean, 2001). Also, differ- Received April 23, 2015; Revised June 27, 2015; Accepted July 21, 2015. ent subsets of cells within the facial motor nucleus are DOI 10.1002/cne.23862 Published online October 8, 2015 in Wiley Online Library VC 2015 Wiley Periodicals, Inc. (wileyonlinelibrary.com) 738 The Journal of Comparative Neurology | Research in Systems Neuroscience 524:738–758 (2016) VGluT1, VGluT2, and VIAAT in orofacial nuclei by sensory feedback (Holstege et al., 1977; Buttner-€ approved by the Ethics Committees of the School of Ennever and Holstege, 1985; Chen et al., 2001; Chen Medicine of the Pontificia Universidad Catolica de Chile, and Travers, 2003; Galvin et al., 2004; Grillner et al., and of the Comision Nacional de Investigacion Cientıf- 2005; Landers and Philip Zeigler, 2006; Nistri et al., ica y Tecnologica CONICYT, both of which conform to 2006; Kinzeler and Travers, 2008; Bianchi and Ges- the guidelines of US National Institutes of Health (NIH) treau, 2009; Moore et al., 2013). Excitatory and inhibi- on animal procedures. Animals were anesthetized with tory neurons located in the midbrain, pontine, and gaseous isoflurane followed by intraperitoneal keta- medullary reticular formation constitute the main pre- mine/xylazine (150 mg/kg and 10 mg/kg, respec- motor afferents to these nuclei, along with primary exci- tively), and then intracardially perfused with phosphate- tatory afferents and various second-order sensory buffered saline (PBS) and 4% paraformaldehyde using a brainstem nuclei (Travers and Norgren, 1983; Nakamura peristaltic pump (Masterflex 7518-00). The brains were and Katakura, 1995; Travers, 2004; Grillner et al., extracted and postfixed for 8 hours in 4% paraformalde- 2005; Takatoh et al., 2013; Stanek Iv et al., 2014). It is hyde, cryoprotected in 30% sucrose, and then cut in expected that the variety of functions and activity pat- 40-lm-thick sections (one of the brains was cut in the terns displayed by the neurons in the different orofacial sagittal plane and the other five were cut in the coronal motor nuclei will be reflected in the type and organiza- plane) using a microtome (Reichert-Jung Hn40, Depew, tion of their afferents. NY) equipped with a freezing stage (Hacker Instruments Previous quantitative analyses on the overall glutama- 220–240v, Fairfield, NJ). Sections from each brain were tergic, GABAergic, and glycinergic innervation of oromo- collected in four series (160 lm between sections in tor neurons have only been done in trigeminal each series) and stored in PBS. motoneurons of cats (Bae et al., 1999; Shigenaga et al., 2005; Shigenaga et al., 2007) and rats (Saha Immunohistochemistry et al., 1991; Yang et al., 1997; Bae et al., 2002). No Antibodies characterization quantitative analyses have been done on the innerva- Primary antibodies used in this study are listed in Table tion of other orofacial motoneurons to allow for com- 1. The rabbit polyclonal anti-VGluT1 antibody (Mab parisons across nuclei. Furthermore, studies on the Technologies, Cat. no. VGT1-3, AB_2315551) was innervation of orofacial motoneurons of the mouse, per- raised against a peptide of the rat VGluT1 (amino acids haps the most important animal model for neuroscience 543–560), which is highly conserved in the mouse nowadays, are still lacking. VGluT1 sequence. This antibody was characterized by With the aim of providing a quantitative description Villalba et al. (2006) in rat and monkey tissue. Western of the main afferents received by each of the orofacial blot analysis showed that anti-VGluT1 labels bands at motor nuclei, we assessed their glutamatergic and 60 kDa, the predicted molecular weight of VGluT1 GABA/glycinergic innervation in the mouse. We used (Villalba et al., 2006). Furthermore, immunostaining is an unbiased stereological technique, the optical fractio- abolished when the antibody is preadsorbed with the nator (West et al., 1991), to estimate the number of peptide (Villalba et al., 2006). The rabbit polyclonal cells and varicosities immunopositive for the vesicular anti-VGluT2 antibody (Synaptic Systems, Goettingen, Germany, Cat. no. 135 403, AB_2254574) was raised transporters for glutamate (VGluT1 and VGluT2) and the against a Strep-TagVR fusion protein of rat VgluT2 vesicular transporter for GABA and glycine (vesicular (amino acids 510–582), and it was characterized by inhibitory amino acid transporter, VIAAT; also known as Hrabovszky et al. (2004) in rat tissue. Immunostaining vesicular GABA transporter, VGAT) in each of these is abolished when the antibody is preadsorbed with the nuclei and their main subdivisions. Finally, we estimated immunization antigen (Hrabovszky, 2004). In addition, the distribution of varicosities over somatic compart- double immunofluorescence assays show that this anti- ments for each vesicular transporter and compared this body and a guinea pig anti VGluT2 produce identical to the overall pattern of innervation within and across labeling (Hrabovszky, 2004). The rabbit anti-VIAAT anti- nuclei. body (VGAT, Synaptic Systems, Cat. no. 131 013, RRID: AB_1966444) was raised against a Strep-TagVR fusion MATERIALS AND METHODS protein of rat VIAAT (amino acids 2–115), and it labels Animals and tissue preparation a band at 55 kDa on western blots of rat hippocam- Six male adult (2 months old) C57BL/6 mice, pus, the predicted molecular weight of VGAT (Stensrud obtained from the animal facility of the Faculty of Bio- et al., 2013). The goat anti-ChAT (Millipore, Bedford, logical
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