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Published in: Brain Structure and Function 1/2022

01-01-2022 | Original Article

Efferent and afferent connections of supratrigeminal neurons conveying orofacial muscle proprioception in rats

Authors: Atsushi Yoshida, Misaki Inoue, Fumihiko Sato, Yayoi Morita, Yumi Tsutsumi, Takahiro Furuta, Katsuro Uchino, Fatema Akhter, Yong Chul Bae, Yoshihisa Tachibana, Tomio Inoue

Published in: Brain Structure and Function | Issue 1/2022

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Abstract

The supratrigeminal nucleus (Su5) is a key structure for controlling jaw movements; it receives proprioceptive sensation from jaw-closing muscle spindles (JCMSs) and sends projections to the trigeminal motor nucleus (Mo5). However, the central projections and regulation of JCMS proprioceptive sensation are not yet fully understood. Therefore, we aimed to reveal the efferent and afferent connections of the Su5 using neuronal tract tracings. Anterograde tracer injections into the Su5 revealed that the Su5 sends contralateral projections (or bilateral projections with a contralateral predominance) to the Su5, basilar pontine nuclei, pontine reticular nucleus, deep mesencephalic nucleus, superior colliculus, caudo-ventromedial edge of the ventral posteromedial thalamic nucleus, parafascicular thalamic nucleus, zona incerta, and lateral hypothalamus, and ipsilateral projections (or bilateral projections with an ipsilateral predominance) to the intertrigeminal region, trigeminal oral subnucleus, dorsal medullary reticular formation, and hypoglossal nucleus as well as the Mo5. Retrograde tracer injections into the Su5 demonstrated that the Su5 receives bilateral projections with a contralateral predominance (or contralateral projections) from the primary and secondary somatosensory cortices, granular insular cortex, and Su5, and ipsilateral projections (or bilateral projections with an ipsilateral predominance) from the dorsal peduncular cortex, bed nuclei of stria terminalis, central amygdaloid nucleus, lateral hypothalamus, parasubthalamic nucleus, trigeminal mesencephalic nucleus, parabrachial nucleus, juxtatrigeminal region, trigeminal oral and caudal subnuclei, and dorsal medullary reticular formation. These findings suggest that the Su5, which receives JCMS proprioception, has efferent and afferent connections with multiple brain regions that are involved in emotional and autonomic functions as well as orofacial motor functions.
Literature
go back to reference Akhter F, Haque T, Sato F, Kato T, Ohara H, Fujio T, Tsutsumi K, Uchino K, Sessle BJ, Yoshida A (2014) Projections from the dorsal peduncular cortex to the trigeminal subnucleus caudalis (medullary dorsal horn) and other lower brainstem areas in rats. Neuroscience 266:23–37PubMed Akhter F, Haque T, Sato F, Kato T, Ohara H, Fujio T, Tsutsumi K, Uchino K, Sessle BJ, Yoshida A (2014) Projections from the dorsal peduncular cortex to the trigeminal subnucleus caudalis (medullary dorsal horn) and other lower brainstem areas in rats. Neuroscience 266:23–37PubMed
go back to reference Alden M, Besson JM, Bernard JF (1994) Organization of the efferent projections from the pontine parabrachial area to the bed nucleus of the stria terminalis and neighboring regions: a PHA-L study in the rat. J Comp Neurol 341:289–314PubMed Alden M, Besson JM, Bernard JF (1994) Organization of the efferent projections from the pontine parabrachial area to the bed nucleus of the stria terminalis and neighboring regions: a PHA-L study in the rat. J Comp Neurol 341:289–314PubMed
go back to reference Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR (1989) Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248–268PubMed Altschuler SM, Bao XM, Bieger D, Hopkins DA, Miselis RR (1989) Viscerotopic representation of the upper alimentary tract in the rat: sensory ganglia and nuclei of the solitary and spinal trigeminal tracts. J Comp Neurol 283:248–268PubMed
go back to reference Arts MPM, Bemelmans FFJ, Cools AR (1998) Role of the retrorubral nucleus in striatally elicited orofacial dyskinesia in cats: effects of muscimol and bicuculline. Psychopharmacol 140:150–156 Arts MPM, Bemelmans FFJ, Cools AR (1998) Role of the retrorubral nucleus in striatally elicited orofacial dyskinesia in cats: effects of muscimol and bicuculline. Psychopharmacol 140:150–156
go back to reference Åström KE (1953) On the central course of afferent fibres in the trigeminal, facial, glossopharyngeal, and vagal nerves and their nuclei in the mouse. Acta Physiol Scand 39(Suppl 106):209–320 Åström KE (1953) On the central course of afferent fibres in the trigeminal, facial, glossopharyngeal, and vagal nerves and their nuclei in the mouse. Acta Physiol Scand 39(Suppl 106):209–320
go back to reference Augustine JR (1985) The insular lobe in primates including humans. Neurol Res 7:2–10PubMed Augustine JR (1985) The insular lobe in primates including humans. Neurol Res 7:2–10PubMed
go back to reference Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229–244PubMed Augustine JR (1996) Circuitry and functional aspects of the insular lobe in primates including humans. Brain Res Brain Res Rev 22:229–244PubMed
go back to reference Avivi-Arber L, Lee JC, Sessle BJ (2010) Effects of incisor extraction on jaw and tongue motor representations within face sensorimotor cortex of adult rats. J Comp Neurol 518:1030–1045PubMed Avivi-Arber L, Lee JC, Sessle BJ (2010) Effects of incisor extraction on jaw and tongue motor representations within face sensorimotor cortex of adult rats. J Comp Neurol 518:1030–1045PubMed
go back to reference Berendse HW, Groenewegen HJ (1991) Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42:73–102PubMed Berendse HW, Groenewegen HJ (1991) Restricted cortical termination fields of the midline and intralaminar thalamic nuclei in the rat. Neuroscience 42:73–102PubMed
go back to reference Bickford ME, Hall WC (1992) The nigral projection to predorsal bundle cells in the superior colliculus of the rat. J Comp Neurol 319:11–33PubMed Bickford ME, Hall WC (1992) The nigral projection to predorsal bundle cells in the superior colliculus of the rat. J Comp Neurol 319:11–33PubMed
go back to reference Bienkowski MS, Rinaman L (2013) Common and distinct neural inputs to the medial central nucleus of the amygdala and anterior ventrolateral bed nucleus of stria terminalis in rats. Brain Struct Funct 218:187–208PubMed Bienkowski MS, Rinaman L (2013) Common and distinct neural inputs to the medial central nucleus of the amygdala and anterior ventrolateral bed nucleus of stria terminalis in rats. Brain Struct Funct 218:187–208PubMed
go back to reference Brodal P (1982) The cerebropontocerebellar pathway: Salient features of its organization. Exp Brain Res [suppl] 6:108–133 Brodal P (1982) The cerebropontocerebellar pathway: Salient features of its organization. Exp Brain Res [suppl] 6:108–133
go back to reference Campbell SK, Parker TD, Welker W (1974) Somatotopic organization of the external cuneate nucleus in albino rats. Brain Res 77:1–23PubMed Campbell SK, Parker TD, Welker W (1974) Somatotopic organization of the external cuneate nucleus in albino rats. Brain Res 77:1–23PubMed
go back to reference Chang Z, Haque T, Iida C, Seki S, Sato F, Kato T, Uchino K, Ono T, Nakamura M, Bae YC, Yoshida A (2009) Distribution of premotoneurons for jaw-closing and jaw-opening motor nucleus receiving contacts from axon terminals of primary somatosensory cortical neurons in rats. Brain Res 1275:43–53PubMed Chang Z, Haque T, Iida C, Seki S, Sato F, Kato T, Uchino K, Ono T, Nakamura M, Bae YC, Yoshida A (2009) Distribution of premotoneurons for jaw-closing and jaw-opening motor nucleus receiving contacts from axon terminals of primary somatosensory cortical neurons in rats. Brain Res 1275:43–53PubMed
go back to reference Coote JH (2005) A role for the paraventricular nucleus of the hypothalamus in the autonomic control of heart and kidney. Exp Physiol 90:169–173PubMed Coote JH (2005) A role for the paraventricular nucleus of the hypothalamus in the autonomic control of heart and kidney. Exp Physiol 90:169–173PubMed
go back to reference Cunningham ET Jr, Sawchenko PE (2000) Dorsal medullary pathways subserving oromotor reflexes in the rat: implications for the central neural control of swallowing. J Comp Neurol 417:448–466PubMed Cunningham ET Jr, Sawchenko PE (2000) Dorsal medullary pathways subserving oromotor reflexes in the rat: implications for the central neural control of swallowing. J Comp Neurol 417:448–466PubMed
go back to reference de No ́RL (1922) Contribucio ́na1conocimientodelnervio trige ́mino. Libro en honor de Dn. S. Ramo ́n y Cajal. Madrid, Mo ́ya 2:13 de No ́RL (1922) Contribucio ́na1conocimientodelnervio trige ́mino. Libro en honor de Dn. S. Ramo ́n y Cajal. Madrid, Mo ́ya 2:13
go back to reference de No ́RL (1933) Vestibulo-ocular reflex arc. Arch Neurol Psychiat 30:245–291 de No ́RL (1933) Vestibulo-ocular reflex arc. Arch Neurol Psychiat 30:245–291
go back to reference Dong HW, Swanson LW (2003) Projections from the rhomboid nucleus of the bed nuclei of the stria terminalis: implications for cerebral hemisphere regulation of ingestive behaviors. J Comp Neurol 463:434–472PubMed Dong HW, Swanson LW (2003) Projections from the rhomboid nucleus of the bed nuclei of the stria terminalis: implications for cerebral hemisphere regulation of ingestive behaviors. J Comp Neurol 463:434–472PubMed
go back to reference Donga R, Lund JP, Veilleux D (1990) An electrophysiological study of trigeminal commissural interneurons in the anaesthetized rabbit. Brain Res 515:351–354PubMed Donga R, Lund JP, Veilleux D (1990) An electrophysiological study of trigeminal commissural interneurons in the anaesthetized rabbit. Brain Res 515:351–354PubMed
go back to reference Donoghue JP, Parham C (1983) Afferent connections of the lateral agranular field of the rat motor cortex. J Comp Neurol 217:390–404PubMed Donoghue JP, Parham C (1983) Afferent connections of the lateral agranular field of the rat motor cortex. J Comp Neurol 217:390–404PubMed
go back to reference Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76–88PubMed Donoghue JP, Wise SP (1982) The motor cortex of the rat: cytoarchitecture and microstimulation mapping. J Comp Neurol 212:76–88PubMed
go back to reference Dubner R, Sessle BJ, Storey AT (1978) The Neural Basis of Oral and Facial Function. Plenum Press, New York Dubner R, Sessle BJ, Storey AT (1978) The Neural Basis of Oral and Facial Function. Plenum Press, New York
go back to reference Fujio T, Sato F, Tachibana Y, Kato T, Tomita A, Higashiyama K, Ono T, Maeda Y, Yoshida A (2016) Revisiting the supratrigeminal nucleus in the rat. Neuroscience 324:307–320PubMed Fujio T, Sato F, Tachibana Y, Kato T, Tomita A, Higashiyama K, Ono T, Maeda Y, Yoshida A (2016) Revisiting the supratrigeminal nucleus in the rat. Neuroscience 324:307–320PubMed
go back to reference Gauriau C, Bernard JF (2004) Posterior triangular thalamic neurons convey nociceptive messages to the secondary somatosensory and insular cortices in the rat. J Neurosci 24:752–761PubMedPubMedCentral Gauriau C, Bernard JF (2004) Posterior triangular thalamic neurons convey nociceptive messages to the secondary somatosensory and insular cortices in the rat. J Neurosci 24:752–761PubMedPubMedCentral
go back to reference Goldberg LJ, Nakamura Y (1968) Lingually induced inhibition of masseteric motoneurones. Experientia 24:371–373PubMed Goldberg LJ, Nakamura Y (1968) Lingually induced inhibition of masseteric motoneurones. Experientia 24:371–373PubMed
go back to reference Goto M, Swanson LW (2004) Axonal projections from the parasubthalamic nucleus. J Comp Neurol 469:581–607PubMed Goto M, Swanson LW (2004) Axonal projections from the parasubthalamic nucleus. J Comp Neurol 469:581–607PubMed
go back to reference Graeff FG, Guimarães FS, De Andrade TG, Deakin JF (1996) Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54:129–141PubMed Graeff FG, Guimarães FS, De Andrade TG, Deakin JF (1996) Role of 5-HT in stress, anxiety, and depression. Pharmacol Biochem Behav 54:129–141PubMed
go back to reference Hanamori T, Kunitake T, Kato K, Kannan H (1998a) Neurons in the posterior insular cortex are responsive to gustatory stimulation of the pharyngolarynx, baroreceptor and chemoreceptor stimulation, and tail pinch in rats. Brain Res 785:97–106PubMed Hanamori T, Kunitake T, Kato K, Kannan H (1998a) Neurons in the posterior insular cortex are responsive to gustatory stimulation of the pharyngolarynx, baroreceptor and chemoreceptor stimulation, and tail pinch in rats. Brain Res 785:97–106PubMed
go back to reference Hanamori T, Kunitake T, Kato K, Kannan H (1998b) Responses of neurons in the insular cortex to gustatory, visceral, and nociceptive stimuli in rats. J Neurophysiol 79:2535–2545PubMed Hanamori T, Kunitake T, Kato K, Kannan H (1998b) Responses of neurons in the insular cortex to gustatory, visceral, and nociceptive stimuli in rats. J Neurophysiol 79:2535–2545PubMed
go back to reference Haque T, Akhter F, Kato T, Sato F, Takeda R, Higashiyama K, Moritani M, Bae YC, Sessle BJ, Yoshida A (2012) Somatotopic direct projections from orofacial areas of secondary somatosensory cortex to trigeminal sensory nuclear complex in rats. Neuroscience 219:214–233PubMed Haque T, Akhter F, Kato T, Sato F, Takeda R, Higashiyama K, Moritani M, Bae YC, Sessle BJ, Yoshida A (2012) Somatotopic direct projections from orofacial areas of secondary somatosensory cortex to trigeminal sensory nuclear complex in rats. Neuroscience 219:214–233PubMed
go back to reference Hattox AM, Priest CA, Keller A (2002) Functional circuitry involved in the regulation of whisker movements. J Comp Neurol 442:266–276PubMedPubMedCentral Hattox AM, Priest CA, Keller A (2002) Functional circuitry involved in the regulation of whisker movements. J Comp Neurol 442:266–276PubMedPubMedCentral
go back to reference Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78–84PubMed Herman JP, Cullinan WE (1997) Neurocircuitry of stress: central control of the hypothalamo-pituitary-adrenocortical axis. Trends Neurosci 20:78–84PubMed
go back to reference Hicks RR, Huerta MF (1991) Differential thalamic connectivity of rostral and caudal parts of cortical area Fr2 in rats. Brain Res 568:325–329PubMed Hicks RR, Huerta MF (1991) Differential thalamic connectivity of rostral and caudal parts of cortical area Fr2 in rats. Brain Res 568:325–329PubMed
go back to reference Huerta MF, Harting JK (1984) Connectional organization of the superior colliculus. Trends Neurosci 7:286–289 Huerta MF, Harting JK (1984) Connectional organization of the superior colliculus. Trends Neurosci 7:286–289
go back to reference Ikenoue E, Akhter F, Tsutsumi Y, Sato F, Ohara H, Uchino K, Furuta T, Tachibana Y, Yoshida A (2018) Transcortical descending pathways through granular insular cortex conveying orofacial proprioception. Brain Res 1687:11–19PubMed Ikenoue E, Akhter F, Tsutsumi Y, Sato F, Ohara H, Uchino K, Furuta T, Tachibana Y, Yoshida A (2018) Transcortical descending pathways through granular insular cortex conveying orofacial proprioception. Brain Res 1687:11–19PubMed
go back to reference Ito S (1992) Multiple projection of vagal non-myelinated afferents to the anterior insular cortex in rats. Neurosci Lett 148:151–154PubMed Ito S (1992) Multiple projection of vagal non-myelinated afferents to the anterior insular cortex in rats. Neurosci Lett 148:151–154PubMed
go back to reference Jerge CR (1963) The function of the nucleus supratrigeminalis. J Neurophysiol 26:393–402PubMed Jerge CR (1963) The function of the nucleus supratrigeminalis. J Neurophysiol 26:393–402PubMed
go back to reference Kawamura Y, Tsukamoto S (1960) Analysis of jaw movements from the cortical jaw motor area and amygdala. Jpn J Physiol 10:471–488PubMed Kawamura Y, Tsukamoto S (1960) Analysis of jaw movements from the cortical jaw motor area and amygdala. Jpn J Physiol 10:471–488PubMed
go back to reference Kidokoro Y, Kubota K, Shuto S, Sumino R (1968) Possible interneurons responsible for reflex inhibition of motoneurons of jaw-closing muscles from the inferior dental nerve. J Neurophysiol 31:709–716PubMed Kidokoro Y, Kubota K, Shuto S, Sumino R (1968) Possible interneurons responsible for reflex inhibition of motoneurons of jaw-closing muscles from the inferior dental nerve. J Neurophysiol 31:709–716PubMed
go back to reference Kosinski RJ, Neafsey EJ, Castro AJ (1986) A comparative topographical analysis of dorsal column nuclear and cerebral cortical projections to the basilar pontine gray in rats. J Comp Neurol 244:163–173PubMed Kosinski RJ, Neafsey EJ, Castro AJ (1986) A comparative topographical analysis of dorsal column nuclear and cerebral cortical projections to the basilar pontine gray in rats. J Comp Neurol 244:163–173PubMed
go back to reference Landgren S, Olsson KA (1980) The effect of electrical stimulation in the hypothalamus on the monosynaptic jaw closing and the disynaptic jaw opening reflexes in the cat. Exp Brain Res 39:389–400PubMed Landgren S, Olsson KA (1980) The effect of electrical stimulation in the hypothalamus on the monosynaptic jaw closing and the disynaptic jaw opening reflexes in the cat. Exp Brain Res 39:389–400PubMed
go back to reference Li YQ, Takada M, Kaneko T, Mizuno N (1995) Premotor neurons for trigeminal motor nucleus neurons innervating the jaw-closing and jaw-opening muscles: differential distribution in the lower brainstem of the rat. J Comp Neurol 356:563–579PubMed Li YQ, Takada M, Kaneko T, Mizuno N (1995) Premotor neurons for trigeminal motor nucleus neurons innervating the jaw-closing and jaw-opening muscles: differential distribution in the lower brainstem of the rat. J Comp Neurol 356:563–579PubMed
go back to reference Luo P, Wong R, Dessem D (1995) Projection of jaw-muscle spindle afferents to the caudal brainstem in rats demonstrated using intracellular biotinamide. J Comp Neurol 358:63–78PubMed Luo P, Wong R, Dessem D (1995) Projection of jaw-muscle spindle afferents to the caudal brainstem in rats demonstrated using intracellular biotinamide. J Comp Neurol 358:63–78PubMed
go back to reference Luo P, Moritani M, Dessem D (2001) Jaw-muscle spindle afferent pathways to the trigeminal motor nucleus in the rat. J Comp Neurol 435:341–353PubMed Luo P, Moritani M, Dessem D (2001) Jaw-muscle spindle afferent pathways to the trigeminal motor nucleus in the rat. J Comp Neurol 435:341–353PubMed
go back to reference Ma WL, Zhang WB, Xiong KH, Guo F (2007) Visceral and orofacial somatic afferent fiber terminals converge onto the same neuron in paratrigeminal nucleus: An electron microscopic study in rats. Auton Neurosci 131:45–49PubMed Ma WL, Zhang WB, Xiong KH, Guo F (2007) Visceral and orofacial somatic afferent fiber terminals converge onto the same neuron in paratrigeminal nucleus: An electron microscopic study in rats. Auton Neurosci 131:45–49PubMed
go back to reference Malick A, Burstein R (1998) Cells of origin of the trigeminohypothalamic tract in the rat. J Comp Neurol 400:125–144PubMed Malick A, Burstein R (1998) Cells of origin of the trigeminohypothalamic tract in the rat. J Comp Neurol 400:125–144PubMed
go back to reference Malick A, Strassman RM, Burstein R (2000) Trigeminohypothalamic and reticulohypothalamic tract neurons in the upper cervical spinal cord and caudal medulla of the rat. J Neurophysiol 84:2078–2112PubMed Malick A, Strassman RM, Burstein R (2000) Trigeminohypothalamic and reticulohypothalamic tract neurons in the upper cervical spinal cord and caudal medulla of the rat. J Neurophysiol 84:2078–2112PubMed
go back to reference Mascaro MB, Prosdocimi FC, Bittencourt JC, Elias CF (2009) Forebrain projections to brainstem nuclei involved in the control of mandibular movements in rats. Eur J Oral Sci 117:676–684PubMed Mascaro MB, Prosdocimi FC, Bittencourt JC, Elias CF (2009) Forebrain projections to brainstem nuclei involved in the control of mandibular movements in rats. Eur J Oral Sci 117:676–684PubMed
go back to reference Mesulam MM, Mufson EJ (1982) Insula of the old world monkey. III: efferent cortical output and comments on function. J Comp Neurol 212:38–52PubMed Mesulam MM, Mufson EJ (1982) Insula of the old world monkey. III: efferent cortical output and comments on function. J Comp Neurol 212:38–52PubMed
go back to reference Mihailoff GA, Kosinski RJ, Azizi SA, Border BG (1989) Survey of noncortical afferent projections to the basilar pontine nuclei: a retrograde tracing study in the rat. J Comp Neurol 282:617–643PubMed Mihailoff GA, Kosinski RJ, Azizi SA, Border BG (1989) Survey of noncortical afferent projections to the basilar pontine nuclei: a retrograde tracing study in the rat. J Comp Neurol 282:617–643PubMed
go back to reference Mitrofanis J (2005) Some certainty for the “zone of uncertainty”? Exploring the function of the zona incerta. Neuroscience 130:1–15PubMed Mitrofanis J (2005) Some certainty for the “zone of uncertainty”? Exploring the function of the zona incerta. Neuroscience 130:1–15PubMed
go back to reference Miyazaki R, Luschei ES (1987) Responses of neurons in nucleus supratrigeminalis to sinusoidal jaw movements in the cat. Exp Neurol 96:145–157PubMed Miyazaki R, Luschei ES (1987) Responses of neurons in nucleus supratrigeminalis to sinusoidal jaw movements in the cat. Exp Neurol 96:145–157PubMed
go back to reference Mizuno N (1970) Projection fibers from the main sensory trigeminal nucleus and the supratrigeminal region. J Comp Neurol 139:457–471PubMed Mizuno N (1970) Projection fibers from the main sensory trigeminal nucleus and the supratrigeminal region. J Comp Neurol 139:457–471PubMed
go back to reference Nakamura Y, Kubo Y (1978) Masticatory rhythm in intracellular potential of trigeminal motoneurons induced by stimulation of orbital cortex and amygdala in cats. Brain Res 14:504–509 Nakamura Y, Kubo Y (1978) Masticatory rhythm in intracellular potential of trigeminal motoneurons induced by stimulation of orbital cortex and amygdala in cats. Brain Res 14:504–509
go back to reference Nakamura S, Inoue T, Nakajima K, Moritani M, Nakayama K, Tokita K, Yoshida A, Maki K (2008) Synaptic transmission from the supratrigeminal region to jaw-closing and jaw-opening motoneurons in developing rats. J Neurophysiol 100:1885–1896PubMed Nakamura S, Inoue T, Nakajima K, Moritani M, Nakayama K, Tokita K, Yoshida A, Maki K (2008) Synaptic transmission from the supratrigeminal region to jaw-closing and jaw-opening motoneurons in developing rats. J Neurophysiol 100:1885–1896PubMed
go back to reference Nonaka M, Nishimura A, Nakamura S, Nakayama K, Mochizuki A, Iijima T, Inoue T (2012) Convergent pre-motoneuronal inputs to single trigeminal motoneurons. J Dent Res 91:888–893PubMed Nonaka M, Nishimura A, Nakamura S, Nakayama K, Mochizuki A, Iijima T, Inoue T (2012) Convergent pre-motoneuronal inputs to single trigeminal motoneurons. J Dent Res 91:888–893PubMed
go back to reference Notsu K, Tsumori T, Yokota S, Sekine J, Yasui Y (2008) Posterior lateral hypothalamic axon terminals are in contact with trigeminal premotor neurons in the parvicellular reticular formation of the rat medulla oblongata. Brain Res 1244:71–81PubMed Notsu K, Tsumori T, Yokota S, Sekine J, Yasui Y (2008) Posterior lateral hypothalamic axon terminals are in contact with trigeminal premotor neurons in the parvicellular reticular formation of the rat medulla oblongata. Brain Res 1244:71–81PubMed
go back to reference Ogawa H, Wang XD (2002) Neurons in the cortical taste area receive nociceptive inputs from the whole body as well as the oral cavity in the rat. Neurosci Lett 322:87–90PubMed Ogawa H, Wang XD (2002) Neurons in the cortical taste area receive nociceptive inputs from the whole body as well as the oral cavity in the rat. Neurosci Lett 322:87–90PubMed
go back to reference Ohta M, Moriyama Y (1986) Supratrigeminal neurons mediate the shortest, disynaptic pathway from the central amygdaloid nucleus to the contralateral trigeminal motoneurons in the rat. Comp Biochem Physiol A Comp Physiol 83:633–641PubMed Ohta M, Moriyama Y (1986) Supratrigeminal neurons mediate the shortest, disynaptic pathway from the central amygdaloid nucleus to the contralateral trigeminal motoneurons in the rat. Comp Biochem Physiol A Comp Physiol 83:633–641PubMed
go back to reference Oka A, Yamamoto M, Takeda R, Ohara H, Sato F, Akhter F, Haque T, Kato T, Sessle BJ, Takada K, Yoshida A (2013) Jaw-opening and -closing premotoneurons in the nucleus of the solitary tract making contacts with laryngeal and pharyngeal afferent terminals in rats. Brain Res 1540:48–63PubMed Oka A, Yamamoto M, Takeda R, Ohara H, Sato F, Akhter F, Haque T, Kato T, Sessle BJ, Takada K, Yoshida A (2013) Jaw-opening and -closing premotoneurons in the nucleus of the solitary tract making contacts with laryngeal and pharyngeal afferent terminals in rats. Brain Res 1540:48–63PubMed
go back to reference Paik SK, Lee HJ, Choi MK, Cho YS, Park MJ, Moritani M, Yoshida A, Kim YS, Bae YC (2009) Ultrastructural analysis of glutamate-, GABA-, and glycine-immunopositive boutons from supratrigeminal premotoneurons in the rat trigeminal motor nucleus. J Neurosci Res 87:1115–1122PubMed Paik SK, Lee HJ, Choi MK, Cho YS, Park MJ, Moritani M, Yoshida A, Kim YS, Bae YC (2009) Ultrastructural analysis of glutamate-, GABA-, and glycine-immunopositive boutons from supratrigeminal premotoneurons in the rat trigeminal motor nucleus. J Neurosci Res 87:1115–1122PubMed
go back to reference Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, Sydney Paxinos G, Watson C (1986) The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press, Sydney
go back to reference Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, Sydney Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinates, 4th edn. Academic Press, Sydney
go back to reference Paxinos G, Watson C (2014) The Rat Brain in Stereotaxic Coordinates, 7th edn. Academic Press, Sydney Paxinos G, Watson C (2014) The Rat Brain in Stereotaxic Coordinates, 7th edn. Academic Press, Sydney
go back to reference Peters J, Kalivas PW, Quirk GJ (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16:279–288PubMedPubMedCentral Peters J, Kalivas PW, Quirk GJ (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16:279–288PubMedPubMedCentral
go back to reference Phelan KD, Falls WM (1989) The interstitial system of the spinal trigeminal tract in the rat: anatomical evidence for morphological and functional heterogeneity. Somatosens Mot Res 6:367–399PubMed Phelan KD, Falls WM (1989) The interstitial system of the spinal trigeminal tract in the rat: anatomical evidence for morphological and functional heterogeneity. Somatosens Mot Res 6:367–399PubMed
go back to reference Porter JD, Donaldson IM (1991) The anatomical substrate for cat extraocular muscle proprioception. Neuroscience 43:473–483PubMed Porter JD, Donaldson IM (1991) The anatomical substrate for cat extraocular muscle proprioception. Neuroscience 43:473–483PubMed
go back to reference Rokx JT, van Willigen JD, Jüch PJ (1986) Bilateral brainstem connections of the rat supratrigeminal region. Acta Anat (basel) 127:16–21 Rokx JT, van Willigen JD, Jüch PJ (1986) Bilateral brainstem connections of the rat supratrigeminal region. Acta Anat (basel) 127:16–21
go back to reference Rosén I, Sjölund B (1973) Organization of group I activated cells in the main and external cuneate nuclei of the cat: identification of muscle receptors. Exp Brain Res 16:221–237PubMed Rosén I, Sjölund B (1973) Organization of group I activated cells in the main and external cuneate nuclei of the cat: identification of muscle receptors. Exp Brain Res 16:221–237PubMed
go back to reference Sanders KH, Klein CE, Mayor TE, Heym C, Handwerker HO (1980) Differential effects of noxious and non-noxious input on neurones according to location in ventral periaqueductal grey or dorsal raphe nucleus. Brain Res 186:83–97PubMed Sanders KH, Klein CE, Mayor TE, Heym C, Handwerker HO (1980) Differential effects of noxious and non-noxious input on neurones according to location in ventral periaqueductal grey or dorsal raphe nucleus. Brain Res 186:83–97PubMed
go back to reference Sasamoto K, Ohta M (1982) Amygdaloid-induced jaw opening and facilitation or inhibition of the trigeminal motoneurons in the rat. Comp Biochem Physiol A Comp Physiol 73:349–354PubMed Sasamoto K, Ohta M (1982) Amygdaloid-induced jaw opening and facilitation or inhibition of the trigeminal motoneurons in the rat. Comp Biochem Physiol A Comp Physiol 73:349–354PubMed
go back to reference Sasamoto K, Zhang G, Iwasaki M (1990) Two types of rhythmical jaw movements evoked by stimulation of the rat cortex. Jpn J Oral Biol 32:57–68 Sasamoto K, Zhang G, Iwasaki M (1990) Two types of rhythmical jaw movements evoked by stimulation of the rat cortex. Jpn J Oral Biol 32:57–68
go back to reference Sato F, Akhter F, Haque T, Kato T, Takeda R, Nagase Y, Sessle BJ, Yoshida A (2013) Projections from the insular cortex to pain- receptive trigeminal caudal subnucleus (medullary dorsal horn) and other lower brainstem areas in rats. Neuroscience 233:9–27PubMed Sato F, Akhter F, Haque T, Kato T, Takeda R, Nagase Y, Sessle BJ, Yoshida A (2013) Projections from the insular cortex to pain- receptive trigeminal caudal subnucleus (medullary dorsal horn) and other lower brainstem areas in rats. Neuroscience 233:9–27PubMed
go back to reference Sato F, Uemura Y, Kanno C, Tsutsumi Y, Tomita A, Oka A, Kato T, Uchino K, Murakami J, Haque T, Tachibana Y, Yoshida A (2017) Thalamo-insular pathway conveying orofacial muscle proprioception in the rat. Neuroscience 365:158–178PubMed Sato F, Uemura Y, Kanno C, Tsutsumi Y, Tomita A, Oka A, Kato T, Uchino K, Murakami J, Haque T, Tachibana Y, Yoshida A (2017) Thalamo-insular pathway conveying orofacial muscle proprioception in the rat. Neuroscience 365:158–178PubMed
go back to reference Satoh Y, Ishizuka K, Murakami T (2007) Changes in cortically induced rhythmic jaw movements after lesioning of the red nucleus in rats. Brain Res 1165:60–70PubMed Satoh Y, Ishizuka K, Murakami T (2007) Changes in cortically induced rhythmic jaw movements after lesioning of the red nucleus in rats. Brain Res 1165:60–70PubMed
go back to reference Sawchenko PE, Brown ER, Chan RK, Ericsson A, Li HY, Roland BL, Kovacs KJ (1996) The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. Prog Brain Res 107:201–222PubMed Sawchenko PE, Brown ER, Chan RK, Ericsson A, Li HY, Roland BL, Kovacs KJ (1996) The paraventricular nucleus of the hypothalamus and the functional neuroanatomy of visceromotor responses to stress. Prog Brain Res 107:201–222PubMed
go back to reference Shammah-Lagnado SJ, Alheid GF, Heimer L (2001) Striatal and central extended amygdala parts of the interstitial nucleus of the posterior limb of the anterior commissure: evidence from tract-tracing techniques in the rat. J Comp Neurol 439:104–126PubMed Shammah-Lagnado SJ, Alheid GF, Heimer L (2001) Striatal and central extended amygdala parts of the interstitial nucleus of the posterior limb of the anterior commissure: evidence from tract-tracing techniques in the rat. J Comp Neurol 439:104–126PubMed
go back to reference Shigenaga Y, Mitsuhiro Y, Yoshida A, Cao CQ, Tsuru H (1988a) Morphology of single mesencephalic trigeminal neurons innervating masseter muscle of the cat. Brain Res 445:392–399PubMed Shigenaga Y, Mitsuhiro Y, Yoshida A, Cao CQ, Tsuru H (1988a) Morphology of single mesencephalic trigeminal neurons innervating masseter muscle of the cat. Brain Res 445:392–399PubMed
go back to reference Shigenaga Y, Sera M, Nishimori T, Suemune S, Nishimura M, Yoshida A, Tsuru K (1988b) The central projection of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord. J Comp Neurol 268:489–507PubMed Shigenaga Y, Sera M, Nishimori T, Suemune S, Nishimura M, Yoshida A, Tsuru K (1988b) The central projection of masticatory afferent fibers to the trigeminal sensory nuclear complex and upper cervical spinal cord. J Comp Neurol 268:489–507PubMed
go back to reference Shigenaga Y, Doe K, Suemune S, Mitsuhiro Y, Tsuru K, Otani K, Shirana Y, Hosoi M, Yoshida A, Kagawa K (1989) Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat –intra-axonal staining with HRP. Brain Res 505:91–110PubMed Shigenaga Y, Doe K, Suemune S, Mitsuhiro Y, Tsuru K, Otani K, Shirana Y, Hosoi M, Yoshida A, Kagawa K (1989) Physiological and morphological characteristics of periodontal mesencephalic trigeminal neurons in the cat –intra-axonal staining with HRP. Brain Res 505:91–110PubMed
go back to reference Shigenaga Y, Mitsuhiro Y, Shirana Y, Tsuru H (1990) Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP. Brain Res 514:219–237PubMed Shigenaga Y, Mitsuhiro Y, Shirana Y, Tsuru H (1990) Two types of jaw-muscle spindle afferents in the cat as demonstrated by intra-axonal staining with HRP. Brain Res 514:219–237PubMed
go back to reference Shimizu K, Asano M, Kitagawa J, Ogiso B, Ren K, Oki H, Matsumoto M, Iwata K (2006) Phosphorylation of extracellular signal-regulated kinase in medullary and upper cervical cord neurons following noxious tooth pulp stimulation. Brain Res 1072:99–109PubMed Shimizu K, Asano M, Kitagawa J, Ogiso B, Ren K, Oki H, Matsumoto M, Iwata K (2006) Phosphorylation of extracellular signal-regulated kinase in medullary and upper cervical cord neurons following noxious tooth pulp stimulation. Brain Res 1072:99–109PubMed
go back to reference Swanson LW (2004) Brain maps: Structure of the rat brain. A laboratory guide with printed and electronic templates for data, models and schematics (3rd ed.). Elsevier, Amsterdam, The Netherlands Swanson LW (2004) Brain maps: Structure of the rat brain. A laboratory guide with printed and electronic templates for data, models and schematics (3rd ed.). Elsevier, Amsterdam, The Netherlands
go back to reference Swenson RS, Kosinski RJ, Castro AJ (1984) Topography of spinal, dorsal column nuclear, and spinal trigeminal projections to the pontine gray in rats. J Comp Neurol 222:301–311PubMed Swenson RS, Kosinski RJ, Castro AJ (1984) Topography of spinal, dorsal column nuclear, and spinal trigeminal projections to the pontine gray in rats. J Comp Neurol 222:301–311PubMed
go back to reference Takata M, Kawamura Y (1970) Neurophysiologic properties of the supratrigeminal nucleus. Jap J Physiol 20:1–11 Takata M, Kawamura Y (1970) Neurophysiologic properties of the supratrigeminal nucleus. Jap J Physiol 20:1–11
go back to reference Takemura M, Sugimoto T, Shigenaga Y (1991) Difference in central projection of primary afferents innervating facial and intraoral structures in the rat. Exp Neurol 111:324–331PubMed Takemura M, Sugimoto T, Shigenaga Y (1991) Difference in central projection of primary afferents innervating facial and intraoral structures in the rat. Exp Neurol 111:324–331PubMed
go back to reference Taylor A (1990) Neurophysiology of the Jaws and Teeth. Macmillan Press, London Taylor A (1990) Neurophysiology of the Jaws and Teeth. Macmillan Press, London
go back to reference Ter Horst GJ, Copray JC, Liem RS, Van Willigen JD (1991) Projections from the rostral parvocellular reticular formation to pontine and medullary nuclei in the rat: involvement in autonomic regulation and orofacial motor control. Neuroscience 40:735–758PubMed Ter Horst GJ, Copray JC, Liem RS, Van Willigen JD (1991) Projections from the rostral parvocellular reticular formation to pontine and medullary nuclei in the rat: involvement in autonomic regulation and orofacial motor control. Neuroscience 40:735–758PubMed
go back to reference Thompson RH, Swanson LW (2003) Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res Brain Res Rev 41:153–202PubMed Thompson RH, Swanson LW (2003) Structural characterization of a hypothalamic visceromotor pattern generator network. Brain Res Brain Res Rev 41:153–202PubMed
go back to reference Tomita A, Kato T, Sato F, Haque T, Oka A, Yamamoto M, Ono T, Bae YC, Maeda Y, Sessle BJ, Yoshida A (2012) Somatotopic direct projections from orofacial areas of primary somatosensory cortex to pons and medulla, especially to trigeminal sensory nuclear complex, in rats. Neuroscience 200:166–185PubMed Tomita A, Kato T, Sato F, Haque T, Oka A, Yamamoto M, Ono T, Bae YC, Maeda Y, Sessle BJ, Yoshida A (2012) Somatotopic direct projections from orofacial areas of primary somatosensory cortex to pons and medulla, especially to trigeminal sensory nuclear complex, in rats. Neuroscience 200:166–185PubMed
go back to reference Torvik A (1956) Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures. J Comp Neurol 106:51–141PubMed Torvik A (1956) Afferent connections to the sensory trigeminal nuclei, the nucleus of the solitary tract and adjacent structures. J Comp Neurol 106:51–141PubMed
go back to reference Travers JB, Norgren R (1983) Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280–298PubMed Travers JB, Norgren R (1983) Afferent projections to the oral motor nuclei in the rat. J Comp Neurol 220:280–298PubMed
go back to reference Tsutsumi Y, Mizuno Y, Haque H, Sato F, Furuta T, Oka A, Moritani M, Bae YC, Yamashiro T, Tachibana Y, Yoshida A (2021) Widespread corticopetal projections from the oval paracentral nucleus of the intralaminar thalamic nuclei conveying orofacial proprioception in rats. Brain Struct Funct 226:1115–1133PubMed Tsutsumi Y, Mizuno Y, Haque H, Sato F, Furuta T, Oka A, Moritani M, Bae YC, Yamashiro T, Tachibana Y, Yoshida A (2021) Widespread corticopetal projections from the oval paracentral nucleus of the intralaminar thalamic nuclei conveying orofacial proprioception in rats. Brain Struct Funct 226:1115–1133PubMed
go back to reference Uchida T, Adachi K, Fujita S, Lee J, Gionhaku N, Cools AR, Koshikawa N (2005) Role of GABAA receptors in the retrorubral filed and ventral pallidum in rat jaw movements elicited by dopaminergic stimulation of the nucleus accumbens shell. Eur J Pharmacol 510:39–47PubMed Uchida T, Adachi K, Fujita S, Lee J, Gionhaku N, Cools AR, Koshikawa N (2005) Role of GABAA receptors in the retrorubral filed and ventral pallidum in rat jaw movements elicited by dopaminergic stimulation of the nucleus accumbens shell. Eur J Pharmacol 510:39–47PubMed
go back to reference Uchino K, Higashiyama K, Kato T, Haque T, Sato F, Tomita A, Tsutsumi K, Moritani M, Yamamura K, Yoshida A (2015) Jaw movement-related primary somatosensory cortical area in the rat. Brain Res 284:55–64 Uchino K, Higashiyama K, Kato T, Haque T, Sato F, Tomita A, Tsutsumi K, Moritani M, Yamamura K, Yoshida A (2015) Jaw movement-related primary somatosensory cortical area in the rat. Brain Res 284:55–64
go back to reference Uemura Y, Haque T, Sato F, Tsutsumi Y, Ohara H, Oka A, Furuta T, Bae YC, Yamashiro T, Tachibana Y, Yoshida A (2020) Proprioceptive thalamus receiving forelimb and neck muscle spindle inputs via the external cuneate nucleus in the rat. Brain Struct Funct 225:2177–2192PubMed Uemura Y, Haque T, Sato F, Tsutsumi Y, Ohara H, Oka A, Furuta T, Bae YC, Yamashiro T, Tachibana Y, Yoshida A (2020) Proprioceptive thalamus receiving forelimb and neck muscle spindle inputs via the external cuneate nucleus in the rat. Brain Struct Funct 225:2177–2192PubMed
go back to reference Valverde F (1962) Reticular formation of the albino rat’s brain stem cytoarchitecture and corticofugal connections. J Comp Neurol 119:25–53PubMed Valverde F (1962) Reticular formation of the albino rat’s brain stem cytoarchitecture and corticofugal connections. J Comp Neurol 119:25–53PubMed
go back to reference Van Eden CG, Lamme VA, Uylings HB (1992) Heterotopic cortical afferents to the medial prefrontal cortex in the rat. A combined retrograde and anterograde tracer study. Eur J Neurosci 4:77–97PubMed Van Eden CG, Lamme VA, Uylings HB (1992) Heterotopic cortical afferents to the medial prefrontal cortex in the rat. A combined retrograde and anterograde tracer study. Eur J Neurosci 4:77–97PubMed
go back to reference VanderWerf F, Aramideh M, Ongerboer de Visser BW, Baljet B, Speelman JD, Otto AJ (1997) A retrograde double fluorescent tracing study of the levator palpebrae superioris muscle in the cynomolgus monkey. Exp Brain Res 113:174–179PubMed VanderWerf F, Aramideh M, Ongerboer de Visser BW, Baljet B, Speelman JD, Otto AJ (1997) A retrograde double fluorescent tracing study of the levator palpebrae superioris muscle in the cynomolgus monkey. Exp Brain Res 113:174–179PubMed
go back to reference Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ (2006) Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13:728–733PubMedPubMedCentral Vidal-Gonzalez I, Vidal-Gonzalez B, Rauch SL, Quirk GJ (2006) Microstimulation reveals opposing influences of prelimbic and infralimbic cortex on the expression of conditioned fear. Learn Mem 13:728–733PubMedPubMedCentral
go back to reference Weiner S, Shaikh MB, Siegel A (1993) Electromyographic activity in the masseter muscle resulting from stimulation of hypothalamic behavioral sites in the cat. J Orofac Pain 7:370–377PubMed Weiner S, Shaikh MB, Siegel A (1993) Electromyographic activity in the masseter muscle resulting from stimulation of hypothalamic behavioral sites in the cat. J Orofac Pain 7:370–377PubMed
go back to reference Wiesendanger R, Wiesendanger M (1982) The corticopontine system in the rat. II. The Projection Pattern J Comp Neurol 208:227–238PubMed Wiesendanger R, Wiesendanger M (1982) The corticopontine system in the rat. II. The Projection Pattern J Comp Neurol 208:227–238PubMed
go back to reference Yamamoto T, Yuyama N, Kawamura Y (1981) Cortical neurons responding to tactile, thermal and taste stimulations of the rat’s tongue. Brain Res 221:202–206PubMed Yamamoto T, Yuyama N, Kawamura Y (1981) Cortical neurons responding to tactile, thermal and taste stimulations of the rat’s tongue. Brain Res 221:202–206PubMed
go back to reference Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R (1988) Sensory inputs from the oral region to the cerebral cortex in behaving rats: an analysis of unit responses in cortical somatosensory and taste areas during ingestive behavior. J Neurophysiol 60:1303–1321PubMed Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R (1988) Sensory inputs from the oral region to the cerebral cortex in behaving rats: an analysis of unit responses in cortical somatosensory and taste areas during ingestive behavior. J Neurophysiol 60:1303–1321PubMed
go back to reference Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R (1989) Sensory and motor responses of trigeminal and reticular neurons during ingestive behavior in rats. Exp Brain Res 76:386–400PubMed Yamamoto T, Matsuo R, Kiyomitsu Y, Kitamura R (1989) Sensory and motor responses of trigeminal and reticular neurons during ingestive behavior in rats. Exp Brain Res 76:386–400PubMed
go back to reference Yamamoto M, Moritani M, Chang Z, Taki I, Tomita A, Ono T, Bae YC, Shigenaga Y, Yoshida A (2007) The somatotopic organization of trigeminal premotoneurons in the cat brainstem. Brain Res 1149:111–117PubMed Yamamoto M, Moritani M, Chang Z, Taki I, Tomita A, Ono T, Bae YC, Shigenaga Y, Yoshida A (2007) The somatotopic organization of trigeminal premotoneurons in the cat brainstem. Brain Res 1149:111–117PubMed
go back to reference Yasui Y, Kayahara T, Shiroyama T, Nakano K (1993) Neurons in the intertrigeminal region of the rat send projection fibers to the superior colliculus. Neurosci Lett 159:39–42PubMed Yasui Y, Kayahara T, Shiroyama T, Nakano K (1993) Neurons in the intertrigeminal region of the rat send projection fibers to the superior colliculus. Neurosci Lett 159:39–42PubMed
go back to reference Yasui Y, Tsumori T, Ando A, Domoto T, Kayahara T, Nakano K (1994) Descending projections from the superior colliculus to the reticular formation around the motor trigeminal nucleus and the parvicellular reticular formation of the medulla oblongata in the rat. Brain Res 656:420–426PubMed Yasui Y, Tsumori T, Ando A, Domoto T, Kayahara T, Nakano K (1994) Descending projections from the superior colliculus to the reticular formation around the motor trigeminal nucleus and the parvicellular reticular formation of the medulla oblongata in the rat. Brain Res 656:420–426PubMed
go back to reference Yasui Y, Tsumori T, Ando A, Domoto T (1995) Demonstration of axon collateral projections from the substantia nigra pars reticulata to the superior colliculus and the parvicellular reticular formation in the rat. Brain Res 674:122–126PubMed Yasui Y, Tsumori T, Ando A, Domoto T (1995) Demonstration of axon collateral projections from the substantia nigra pars reticulata to the superior colliculus and the parvicellular reticular formation in the rat. Brain Res 674:122–126PubMed
go back to reference Yoshida A, Taki I, Chang Z, Iida C, Haque T, Tomita A, Seki S, Yamamoto S, Masuda Y, Moritani M, Shigenaga Y (2009) Corticofugal projections to trigeminal motoneurons innervating antagonistic jaw muscles in rats as demonstrated by anterograde and retrograde tract tracing. J Comp Neurol 514:368–386PubMed Yoshida A, Taki I, Chang Z, Iida C, Haque T, Tomita A, Seki S, Yamamoto S, Masuda Y, Moritani M, Shigenaga Y (2009) Corticofugal projections to trigeminal motoneurons innervating antagonistic jaw muscles in rats as demonstrated by anterograde and retrograde tract tracing. J Comp Neurol 514:368–386PubMed
go back to reference Yoshida A, Fujio T, Sato F, Ali MS, Haque T, Ohara H, Moritani M, Kato T, Dostrovsky JO, Tachibana Y (2017) Orofacial proprioceptive thalamus of the rat. Brain Struct Funct 222:2655–2669PubMed Yoshida A, Fujio T, Sato F, Ali MS, Haque T, Ohara H, Moritani M, Kato T, Dostrovsky JO, Tachibana Y (2017) Orofacial proprioceptive thalamus of the rat. Brain Struct Funct 222:2655–2669PubMed
go back to reference Zhang GX, Sasamoto K (1990) Projections of two separate cortical areas for rhythmical jaw movements in the rat. Brain Res Bull 24:221–230PubMed Zhang GX, Sasamoto K (1990) Projections of two separate cortical areas for rhythmical jaw movements in the rat. Brain Res Bull 24:221–230PubMed
go back to reference Zhou Q, Imbe H, Dubner R, Ren K (1999) Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: implications for persistent orofacial pain. J Comp Neurol 412:276–291PubMed Zhou Q, Imbe H, Dubner R, Ren K (1999) Persistent Fos protein expression after orofacial deep or cutaneous tissue inflammation in rats: implications for persistent orofacial pain. J Comp Neurol 412:276–291PubMed
Metadata
Title
Efferent and afferent connections of supratrigeminal neurons conveying orofacial muscle proprioception in rats
Authors
Atsushi Yoshida
Misaki Inoue
Fumihiko Sato
Yayoi Morita
Yumi Tsutsumi
Takahiro Furuta
Katsuro Uchino
Fatema Akhter
Yong Chul Bae
Yoshihisa Tachibana
Tomio Inoue
Publication date
01-01-2022
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 1/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-021-02391-9

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