NM  Vol.6 No.1 , March 2015
Control Pathways from the Subcortical Limbic Structures to the Trigeminal Motor System in the Lower Brainstem: A Hodological Review
Author(s) Yukihiko Yasui*
ABSTRACT
The organization of the emotion-related somatic motor behavior, including jaw movements, is governed not only by the cortical limbic system but also by the subcortical limbic system including the amygdala and hypothalamus. GABAergic neurons in the central amygdaloid nucleus (CeA) and glutamatergic neurons in the posterior lateral hypothalamus (PLH) exert inhibitory and excitatory influences, respectively, upon premotor neurons for the motor trigeminal nucleus (Vm) in the parvicellular reticular formation (RFp) of the medulla oblongata. The CeA also has an inhibitory influence on non-dopaminergic (probably GABAergic) neurons in the retrorubral field of the midbrain that send their axons to the RFp. Furthermore, the CeA and lateral hypothalamus including the PLH may also modulate Vm neurons via projections to the mesencephalic trigeminal nucleus which contains the cell bodies of primary afferent neurons conveying inputs from the masticatory muscle spindles or the periodontal ligament receptors to jaw closing motoneurons within the Vm. These pathways from the subcortical limbic structures to the trigeminal motor system in the lower brainstem underlie the regulation of emotional jaw movements.

Cite this paper
Yasui, Y. (2015) Control Pathways from the Subcortical Limbic Structures to the Trigeminal Motor System in the Lower Brainstem: A Hodological Review. Neuroscience and Medicine, 6, 24-34. doi: 10.4236/nm.2015.61005.
References
[1]   Davis, M. (1992) The Role of the Amygdala in Fear and Anxiety. Annual Review of Neuroscience, 15, 353-375.
http://dx.doi.org/10.1146/annurev.ne.15.030192.002033

[2]   Holstege, G. (1991) Descending Motor Pathways and the Spinal Motor System: Limbic and Non-Limbic Components. In: Holstege, G., Ed., Role of the Forebrain in Sensation and Behavior, Elsevier, Amsterdam, 307-421.

[3]   LeDoux, J.E. (2000) Emotion Circuits in the Brain. Annual Review of Neuroscience, 23, 155-184.
http://dx.doi.org/10.1146/annurev.neuro.23.1.155

[4]   Mishima, K., Sasamoto, K. and Ohta, M. (1982) Amygdaloid or Cortical Facilitation of Antidromic Activity of Trigeminal Motoneurons in the Rat. Comparative Biochemistry and Physiology Part A: Physiology, 73, 355-359.
http://dx.doi.org/10.1016/0300-9629(82)90167-0

[5]   Nakamura, Y. and Kubo, Y. (1978) Masticatory Rhythm in Intracellular Potential of Trigeminal Motoneurons Induced by Stimulation of Orbital Cortex and Amygdala in Cats. Brain Research, 148, 504-509.
http://dx.doi.org/10.1016/0006-8993(78)90738-2

[6]   Ohta, M. and Moriyama, Y. (1986) Supratrigeminal Neurons Mediate Shortest, Disynaptic Pathway from the Central Amygdaloid Nucleus to the Contralateral Trigeminal Motoneurons in the Rat. Comparative Biochemistry and Physiology Part A: Physiology, 83, 633-641.
http://dx.doi.org/10.1016/0300-9629(86)90702-4

[7]   Sasamoto, K. and Ohta, M. (1982) Amygdaloid-Induced Jaw Opening and Facilitation or Inhibition of the Trigeminal Motoneurons in the Rat. Comparative Biochemistry and Physiology Part A: Physiology, 73, 349-354.
http://dx.doi.org/10.1016/0300-9629(82)90166-9

[8]   Card, J., Swanson, L.W. and Moore, Y. (2003) The Hypothalamus: An Overview of Regulatory Systems. In: Bloom, F.E., Landis, S.C., Roberts, J.L., Squire, L.R. and Zigmond, M.J., Eds., Fundamental Neuroscience, 2nd Edition, Academic Press, San Diego, 897-909.

[9]   Brody, J.F., DeFeudis, P.A. and DeFeudis, F.V. (1969) Effects of Micro-Injections of L-Glutamate into the Hypothalamus on Attack and Flight Behaviour in Cats. Nature, 224, 1330.
http://dx.doi.org/10.1038/2241330a0

[10]   Brown, J.L., Hunsperger, R.W. and Rosvold, H.E. (1969) Defence, Attack, and Flight Elicited by Electrical Stimulation of the Hypothalamus of the Cat. Experimental Brain Research, 8, 113-129.

[11]   Chi, C.C. and Flynn, J.P. (1971) Neural Pathways Associated with Hypothalamically Elicited Attack Behavior in Cats. Science, 171, 703-706. http://dx.doi.org/10.1126/science.171.3972.703

[12]   Travers, J.B. and Norgren, R. (1983.) Afferent Projections to the Oral Motor Nuclei in the Rat. Journal of Comparative Neurology, 220, 280-298.
http://dx.doi.org/10.1002/cne.902200303

[13]   Li, Y.-Q., Takada, M., Kaneko, T. and 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. Journal of Comparative Neurology, 356, 563-579.
http://dx.doi.org/10.1002/cne.903560407

[14]   Ter Horst, G.J., Copray, J.C.V.M., Liem, R.S.B. and Van Willigen, J.D. (1991) Projections from the Rostral Parvicellular Reticular Formation to Pontine and Medullary Nuclei in the Rat: Involvement in Autonomic Regulation and Orofacial Motor Control. Neuroscience, 40, 735-758.
http://dx.doi.org/10.1016/0306-4522(91)90009-D

[15]   Jerge, C.R. (1963) Organization and Function of the Trigeminal Mesencephalic Nucleus. Journal of Neurophysiology, 26, 379-392.

[16]   Nomura, S. and Mizuno, N. (1985) Differential Distribution of Cell Bodies and Central Axons of Mesencephalic Trigeminal Nucleus Neurons Supplying the Jaw-Closing Muscles and Periodontal Tissue: A Transganglionic Tracer Study in the Cat. Brain Research, 359, 311-319.
http://dx.doi.org/10.1016/0006-8993(85)91442-8

[17]   Liem, R.S., Copray, J.C. and van Willigen, J.D. (1991) Ultrastructure of the Rat Mesencephalic Trigeminal Nucleus. Acta Anatomica, 140, 112-119.
http://dx.doi.org/10.1159/000147045

[18]   Luo, P. and Li, J. (1991) Monosynaptic Connections between Neurons of Trigeminal Mesencephalic Nucleus and Jaw-Closing Motoneurons in the Rat: An Intracellular Horseradish Peroxidase Labeling Study. Brain Research, 559, 267-275.
http://dx.doi.org/10.1016/0006-8993(91)90011-J

[19]   Mascaro, M.B., Bittencourt, J.C., Casatti, C.A. and Elias, C.F. (2005) Alternative Pathways for Catecholamine Action in Oral Motor Control. Neuroscience Letters, 386, 34-39.
http://dx.doi.org/10.1016/j.neulet.2005.05.062

[20]   Yasui, Y., Tsumori, T., Oka, T. and Yokota, S. (2004) Amygdaloid Axon Terminals Are in Contact with Trigeminal Premotor Neurons in the Parvicellular Reticular Formation of the Rat Medulla Oblongata. Brain Research, 1016, 129-134.
http://dx.doi.org/10.1016/j.brainres.2004.04.080

[21]   Lazarov, N.E., Usunoff, K.G., Schmitt, O., Itzev, D.E., Rolfs, A. and Wree, A. (2011) Amygdalotrigeminal Projection in the Rat: An Anterograde Tracing Study. Annals of Anatomy, 193, 118-126.
http://dx.doi.org/10.1016/j.aanat.2010.12.004

[22]   Takeuchi, Y., Satoda, T. and Matsushima, R. (1988) Amygdaloid Projections to the Commissural Interneurons for Masticatory Motoneurons. Brain Research Bulletin, 21, 123-127.
http://dx.doi.org/10.1016/0361-9230(88)90127-X

[23]   Takeuchi, Y., Satoda, T., Tashiro, T., Matsushima, R. and Uemura-Sumi, M. (1988) Amygdaloid Pathway to the Trigeminal Motor Nucleus via the Pontine Reticular Formation in the Rat. Brain Research Bulletin, 21, 829-833.
http://dx.doi.org/10.1016/0361-9230(88)90052-4

[24]   Hopkins, D.A. and Holstege, G. (1978) Amygdaloid Projections to the Mesencephalon, Pons and Medulla Oblongata in the Cat. Experimental Brain Research, 32, 529-547.
http://dx.doi.org/10.1007/BF00239551

[25]   Krettek, J.E. and Price, J.L. (1978) Amygdaloid Projections to Subcortical Structures within the Basal Forebrain and Brainstem in the Rat and Cat. Journal of Comparative Neurology, 178, 225-254.
http://dx.doi.org/10.1002/cne.901780204

[26]   Price, J.L. and Amaral, D.G. (1981) Anautoradiographic Study of the Projections of the Central Nucleus of the Monkey Amygdala. Journal of Neuroscience, 1, 1242-1259.

[27]   Mogoseanu, D., Smith, A.D. and Bolam, J.P. (1993) Monosynaptic Innervation of Trigeminal Motor Neurons Involved in Mastication by Neurons of the Parvicellular Reticular Formation. Journal of Comparative Neurology, 336, 53-65.
http://dx.doi.org/10.1002/cne.903360105

[28]   Yasui, Y., Tsumori, T., Ono, K. and Kishi, T. (1997) Nigral Axon Terminals Are in Contact with Parvicellular Reticular Neurons Which Project to the Motor Trigeminal Nucleus in the Rat. Brain Research, 775, 219-224.
http://dx.doi.org/10.1016/S0006-8993(97)00957-8

[29]   Gonzales, C. and Chesselet, M.F. (1990) Amygdalonigral Pathway: An Anterograde Study in the Rat with Phaseolus vulgaris Leucoagglutinin (PHA-L). Journal of Comparative Neurology, 297, 182-200.
http://dx.doi.org/10.1002/cne.902970203

[30]   Yasui, Y., Nakano, K., Nakagawa, Y., Kayahara, T., Shiroyama, T. and Mizuno, N. (1992) Non-Dopaminergic Neurons in the Substantia Nigra Project to the Reticular Formation around the Trigeminal Motor Nucleus in the Rat. Brain Research, 585, 361-366.
http://dx.doi.org/10.1016/0006-8993(92)91237-9

[31]   Yasui, Y., Tsumori, T., Ando, A. and 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 Research, 674, 122-126.
http://dx.doi.org/10.1016/0006-8993(94)01459-U

[32]   Wallace, D.M., Magnuson, D.J. and Gray, T.S. (1992) Organization of Amygdaloid Projections to Brainstem Dopaminergic, Noradrenergic, and Adrenergic Cell Groups in the Rat. Brain Research Bulletin, 28, 447-454.
http://dx.doi.org/10.1016/0361-9230(92)90046-Z

[33]   Arts, M.P., Bemelmans, F.F. and Cools, A.R. (1998) Role of the Retrorubral Nucleus in Striatally Elicited Orofacial Dyskinesia in Cats: Effects of Muscimol and Bicuculline. Psychopharmacology, 140, 150-156.
http://dx.doi.org/10.1007/s002130050752

[34]   Uchida, T., Adachi, K., Fujita, S., Lee, J., Gionhaku, N., Cools, A.R. and Koshikawa, N. (2005) Role of GABA(A) Receptors in the Retrorubral Field and Ventral Pallidum in Rat Jaw Movements Elicited by Dopaminergic Stimulation of the Nucleus Accumbens Shell. European Journal of Pharmacology, 510, 39-47.
http://dx.doi.org/10.1016/j.ejphar.2005.01.012

[35]   von Krosigk, M. and Smith, A.D. (1991) Descending Projections from the Substantia Nigra and Retrorubral Field to the Medullary and Pontomedullary Reticular Formation. European Journal of Neuroscience, 3, 260-273.
http://dx.doi.org/10.1111/j.1460-9568.1991.tb00088.x

[36]   von Krosigk, M., Smith, Y., Bolam, J.P. and Smith, A.D. (1992) Synaptic Organization of GABAergic Inputs from the Striatum and the Globus Pallidus onto Neurons in the Substantia Nigra and Retrorubral Field Which Project to the Medullary Reticular Formation. Neuroscience, 50, 531-549.
http://dx.doi.org/10.1016/0306-4522(92)90445-8

[37]   Tsumori, T., Qin, Y., Yokota, S., Niu, J.G. and Yasui, Y. (2009) Central Amygdaloid Axon Terminals Are in Contact with Retrorubral Field Neurons That Project to the Parvicellular Reticular Formation of the Medulla Oblongata in the Rat. Brain Research, 1306, 18-28.
http://dx.doi.org/10.1016/j.brainres.2009.09.118

[38]   Mascaro, M.B., Prosdócimi, F.C., Bittencourt, J.C. and Elias, C.F. (2009) Forebrain Projections to Brainstem Nuclei Involved in the Control of Mandibular Movements in Rats. European Journal of Oral Science, 117, 676-684.
http://dx.doi.org/10.1111/j.1600-0722.2009.00686.x

[39]   Shirasu, M., Takahashi, T., Yamamoto, T., Itoh, K., Sato, S. and Nakamura, H. (2011) Direct Projections from the Central Amygdaloid Nucleus to the Mesencephalic Trigeminal Nucleus in Rats. Brain Research, 1400, 19-30.
http://dx.doi.org/10.1016/j.brainres.2011.05.026

[40]   Poulin, J.F., Castonguay-Lebe, Z., Lafores, S. and Drolet, G. (2008) Enkephalin Co-Expression with Classic Neurotransmitters in the Amygdaloid Complex of the Rat. Journal of Comparative Neurology, 506, 943-959.
http://dx.doi.org/10.1002/cne.21587

[41]   Oka, T., Tsumori, T., Yokota, S. and Yasui, Y. (2008) Neuroanatomical and Neurochemical Organization of Projections from the Central Amygdaloid Nucleus to the Nucleus Retroambiguus via the Periaqueductal Gray in the Rat. Neuroscience Research, 62, 286-298.
http://dx.doi.org/10.1016/j.neures.2008.10.004

[42]   Jia, H.G., Zhang, G.Y. and Wan, Q. (2005) A GABAergic Projection from the Central Nucleus of the Amygdala to the Parabrachial Nucleus: An Ultrastructural Study of Anterograde Tracing in Combination with Post-Embedding Immunocytochemistry in the Rat. Neuroscience Letters, 382, 153-157.
http://dx.doi.org/10.1016/j.neulet.2005.03.013

[43]   Jia, H.-G., Rao, Z.-R. and Shi, J.-W. (1997) Evidence of Gamma-Aminobutyricacidergic Control over the Catecholaminergic Projection from the Medulla Oblongata to the Central Nucleus of the Amygdala. Journal of Comparative Neurology, 381, 262-281.
http://dx.doi.org/10.1002/(SICI)1096-9861(19970512)381:3<262::AID-CNE2>3.0.CO;2-0

[44]   Saha, S., Batten, T.F. and Henderson, Z. (2000) A GABAergic Projection from the Central Nucleus of the Amygdala to the Nucleus of the Solitary Tract: A Combined Anterograde Tracing and Electron Microscopic Immunohistochemical Study. Neuroscience, 99, 613-626.
http://dx.doi.org/10.1016/S0306-4522(00)00240-2

[45]   Tsubouchi, K., Tsumori, T., Yokota, S., Okunishi, H. and Yasui, Y. (2007) A Disynaptic Pathway from the Central Amygdaloid Nucleus to the Paraventricular Hypothalamic Nucleus via the Parastrial Nucleus in the Rat. Neuroscience Research, 59, 390-398.
http://dx.doi.org/10.1016/j.neures.2007.08.010

[46]   Tsumori, T., Yokota, S., Qin, Y., Oka, T. and Yasui, Y. (2006) A Light and Electron Microscopic Analysis of the Convergent Insular Cortical and Amygdaloid Projections to the Posterior Lateral Hypothalamus in the Rat, with Special Reference to Cardiovascular Function. Neuroscience Research, 56, 261-269.
http://dx.doi.org/10.1016/j.neures.2006.07.005

[47]   Nakamura, S., Tsumori, T., Yokota, S., Oka, T. and Yasui, Y. (2009) Amygdaloid Axons Innervate Melanin-Concentrating Hormone- and Orexin-Containing Neurons in the Mouse Lateral Hypothalamus. Brain Research, 1278, 66-74.
http://dx.doi.org/10.1016/j.brainres.2009.04.049

[48]   Yasui, Y., Nakano, K., Kayahara, T. and Mizuno, N. (1991) Non-Dopaminergic Projections from the Substantia Nigra Pars Lateralis to the Inferior Colliculus in the Rat. Brain Research, 559, 139-144.
http://dx.doi.org/10.1016/0006-8993(91)90296-8

[49]   Mugnaini, E. and Oertel, W.H. (1985) Atlas of the Distribution of GABAergic Neurons and Terminals in the Rat as Revealed by GAD Immunoreactivity. In: Bjorklund, A. and Hokfelt, T., Eds., Handbook of Chemical Neuroanatomy: GABA and Neuropeptides in the CNS, Part 1, Vol. 4, Elsevier, Amsterdam, 436-595.

[50]   Travers, J.B., Yoo, J.E., Chandran, R., Herman, K. and Travers, S.P. (2005) Neurotransmitter Phenotypes of Intermediate Zone Reticular Formation Projections to the Motor Trigeminal and Hypoglossal Nuclei in the Rat. Journal of Comparative Neurology, 488, 28-47.
http://dx.doi.org/10.1002/cne.20604

[51]   Pang, Y.W., Ge, S.N., Nakamura, K.C., Li, J.L., Xiong, K.H., Kaneko, T. and Mizuno, N. (2009) Axon Terminals Expressing Vesicular Glutamate Transporter VGLUT1 or VGLUT2 within the Trigeminalmotor Nucleus of the Rat: Origins and Distribution Patterns. Journal of Comparative Neurology, 512, 595-612.
http://dx.doi.org/10.1002/cne.21894

[52]   Li, Y.Q., Takada, M., Kaneko, T. and Mizuno, N. (1996) GABAergic and Glycinergic Neurons Projecting to the Trigeminalmotor Nucleus: A Double Labeling Study in the Rat. Journal of Comparative Neurology, 373, 498-510.
http://dx.doi.org/10.1002/(SICI)1096-9861(19960930)373:4<498::AID-CNE3>3.0.CO;2-X

[53]   Kaneko, T., Itoh, K., Shigemoto, R. and Mizuno, N. (1989) Glutaminase-Like Immunoreactivity in the Lower Brainstem and Cerebellum of the Adult Rat. Neuroscience, 32, 79-98.
http://dx.doi.org/10.1016/0306-4522(89)90109-7

[54]   Chen, P., Li, J.-L., Li, J.-S. and Mizuno, N. (2001) Glutamic Acid Decarboxylase-Like Immunoreactive Axon Terminals in Synaptic Contact with Mesencephalic Trigeminal Nucleus Neurons in the Rat. Neuroscience Letters, 298, 167-170.
http://dx.doi.org/10.1016/S0304-3940(00)01736-5

[55]   Pang, Y.W., Li, J.L., Nakamura, K., Wu, S., Kaneko, T. and Mizuno, N. (2006) Expression of Vesicular Glutamate Transporter 1 Immunoreactivity in Peripheral and Central Endings of Trigeminal Mesencephalic Nucleus Neurons in the Rat. Journal of Comparative Neurology, 498, 129-141.
http://dx.doi.org/10.1002/cne.21047

[56]   McGregor, R., Damián, A., Fabbiani, G., Torterolo, P., Pose, I., Chase, M. and Morales, F.R. (2005) Direct Hypothalamic Innervation of the Trigeminal Motor Nucleus: A Retrograde Tracer Study. Neuroscience, 136, 1073-1081.
http://dx.doi.org/10.1016/j.neuroscience.2005.08.028

[57]   Wang, P.Y. and Zang, F.C. (1995) Outline and Atlas of Learning Rat Brain Slices. Northwest University Press, Xi’an.

[58]   Notsu, K., Tsumori, T., Yokota, S., Sekine, J. and 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 Research, 1244, 71-81.
http://dx.doi.org/10.1016/j.brainres.2008.09.076

[59]   Shammah-Lagnado, S.J., Costa, M.S. and Ricardo, J.A. (1992) Afferent Connections of the Parvocellular Reticular Formation: A Horseradish Peroxidase Study in the Rat. Neuroscience, 50, 403-425.
http://dx.doi.org/10.1016/0306-4522(92)90433-3

[60]   Bourgeais, L., Gauriau, C. and Bernard, J.F. (2001) Projections from the Nociceptive Area of the Central Nucleus of the Amygdala to the Forebrain: A PHA-L Study in the Rat. European Journal of Neuroscience, 14, 229-255.
http://dx.doi.org/10.1046/j.0953-816x.2001.01640.x

[61]   Tsumori, T., Yokota, S., Kishi, T., Qin, Y., Oka, T. and Yasui, Y. (2006) Insular Cortical and Amygdaloid Fibers Are in Contact with Posterolateral Hypothalamic Neurons Projecting to the Nucleus of the Solitary Tract in the Rat. Brain Research, 1070, 139-144.
http://dx.doi.org/10.1016/j.brainres.2005.11.040

[62]   Kaneko, T. and Fujiyama, F. (2002) Complementary Distribution of Vesicular Glutamate. Transporters in the Central Nervous System. Neuroscience Research, 42, 243-250.
http://dx.doi.org/10.1016/S0168-0102(02)00009-3

[63]   Ziegler, D.R., Cullinan, W.E. and Herman, J.P. (2002) Distribution of Vesicular Glutamate Transporter mRNA in Rat Hypothalamus. Journal of Comparative Neurology, 448, 217-229.
http://dx.doi.org/10.1002/cne.10257

[64]   Clarke, N.P., Bolam, J.P. and Bevan, M.D. (1996) Glutamate-Enriched Inputs from the Mesopontine Tegmentum to the Entopeduncular Nucleus in the Rat. European Journal of Neuroscience, 8, 1363-1376.
http://dx.doi.org/10.1111/j.1460-9568.1996.tb01599.x

[65]   Gundersen, V., Ottersen, O.P. and Storm-Mathisen, J. (1996) Selective Excitatory Amino Acid Uptake in Glutamatergic Nerve Terminals and in Glia in the Rat Striatum: Quantitative Electron Microscopic Immunocytochemistry of Exogenous (D)-Aspartate and Endogenous Glutamate and GABA. European Journal Neuroscience, 8, 758-765.
http://dx.doi.org/10.1111/j.1460-9568.1996.tb01261.x

[66]   Tai, Q. and Goshgarian, H.G. (1996) Ultrastructural Quantitative Analysis of Glutamatergic and GABAergic Synaptic Terminals in the Phrenic Nucleus after Spinal Cord Injury. Journal of Comparative Neurology, 372, 343-355.
http://dx.doi.org/10.1002/(SICI)1096-9861(19960826)372:3<343::AID-CNE2>3.0.CO;2-2

[67]   Fujiyama, F., Hioki, H., Tomioka, R., Taki, K., Tamamaki, N., Nomura, S., Okamoto, K. and Kaneko, T. (2003) Changes of Immunocytochemical Localization of Vesicular Glutamate Transporters in the Rat Visual System after the Retinofugal Denervation. Journal of Comparative Neurology, 465, 234-249.
http://dx.doi.org/10.1002/cne.10848

[68]   Fung, S.J., Yamuy, J., Sampogna, S., Morales, F.R. and Chase, M.H. (2001) Hypocretin (Orexin) Input to Trigeminal and Hypoglossal Motoneurons in the Cat: A Double-Labeling Immunohistochemical Study. Brain Research, 903, 257-262.
http://dx.doi.org/10.1016/S0006-8993(01)02318-6

[69]   Zhang, J. and Luo, P. (2002) Orexin B Immunoreactive Fibers and Terminals Innervate the Sensory and Motor Neurons of Jaw-Elevator Muscles in the Rat. Synapse, 44, 106-110.
http://dx.doi.org/10.1002/syn.10050

[70]   Saito, Y., Cheng, M., Leslie, F.M. and Civelli, O. (2001) Expression of the Melanin-Concentrating Hormone (MCH) Receptor mRNA in the Rat Brain. Journal of Comparative Neurology, 435, 26-40.
http://dx.doi.org/10.1002/cne.1191

[71]   Holstege, G. (1992) The Emotional Motor System. European Journal of Morphology, 30, 67-79.

[72]   Holstege, G. (2010) The Emotional Motor System and Micturition Control. Neurology and Urodynamics, 29, 42-48.
http://dx.doi.org/10.1002/nau.20789

 
 
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