Forebrain projection neurons target functionally diverse respiratory control areas in the midbrain, pons, and medulla oblongata.
delta
forebrain projection neurons
orofacial motor behaviors
postinspiration
pyramidal neurons
respiratory pattern generation
theta
volitional control of breathing
Journal
The Journal of comparative neurology
ISSN: 1096-9861
Titre abrégé: J Comp Neurol
Pays: United States
ID NLM: 0406041
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
revised:
25
11
2020
received:
21
08
2020
accepted:
29
11
2020
pubmed:
20
12
2020
medline:
27
1
2022
entrez:
19
12
2020
Statut:
ppublish
Résumé
Eupnea is generated by neural circuits located in the ponto-medullary brainstem, but can be modulated by higher brain inputs which contribute to volitional control of breathing and the expression of orofacial behaviors, such as vocalization, sniffing, coughing, and swallowing. Surprisingly, the anatomical organization of descending inputs that connect the forebrain with the brainstem respiratory network remains poorly defined. We hypothesized that descending forebrain projections target multiple distributed respiratory control nuclei across the neuroaxis. To test our hypothesis, we made discrete unilateral microinjections of the retrograde tracer cholera toxin subunit B in the midbrain periaqueductal gray (PAG), the pontine Kölliker-Fuse nucleus (KFn), the medullary Bötzinger complex (BötC), pre-BötC, or caudal midline raphé nuclei. We quantified the regional distribution of retrogradely labeled neurons in the forebrain 12-14 days postinjection. Overall, our data reveal that descending inputs from cortical areas predominantly target the PAG and KFn. Differential forebrain regions innervating the PAG (prefrontal, cingulate cortices, and lateral septum) and KFn (rhinal, piriform, and somatosensory cortices) imply that volitional motor commands for vocalization are specifically relayed via the PAG, while the KFn may receive commands to coordinate breathing with other orofacial behaviors (e.g., sniffing, swallowing). Additionally, we observed that the limbic or autonomic (interoceptive) systems are connected to broadly distributed downstream bulbar respiratory networks. Collectively, these data provide a neural substrate to explain how volitional, state-dependent, and emotional modulation of breathing is regulated by the forebrain.
Substances chimiques
Radioactive Tracers
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2243-2264Informations de copyright
© 2020 Wiley Periodicals LLC.
Références
Aleksandrov, V. G., Aleksandrova, N. P., & Bagaev, V. A. (2000). Identification of a respiratory related area in the rat insular cortex. Canadian Journal of Physiology and Pharmacology, 78(7), 582-586. https://doi.org/10.1139/y00-031.
Bandler, R., & Carrive, P. (1988). Integrated defence reaction elicited by excitatory amino acid microinjection in the midbrain periaqueductal grey region of the unrestrained cat. Brain Research, 439(1-2), 95-106. https://doi.org/10.1016/0006-8993(88)91465-5.
Bandler, R., Carrive, P., & Depaulis, A. (1991). Emerging principles of organization of the midbrain periaqueductal gray matter. In The midbrain periaqueductal gray matter (pp. 1-8). Springer.
Bandler, R., Keay, K. A., Floyd, N., & Price, J. (2000). Central circuits mediating patterned autonomic activity during active vs. passive emotional coping. Brain Research Bulletin, 53(1), 95-104. https://doi.org/10.1016/S0361-9230(00)00313-0.
Bautista, T. G., & Dutschmann, M. (2014). Ponto-medullary nuclei involved in the generation of sequential pharyngeal swallowing and concomitant protective laryngeal adduction in situ. The Journal of Physiology, 592(12), 2605-2623. https://doi.org/10.1113/jphysiol.2014.272468.
Benarroch, E. E. (2012). Periaqueductal gray: An interface for behavioral control. Neurology, 78(3), 210-217. https://doi.org/10.1212/WNL.0b013e31823fcdee.
Besnard, S., Denise, P., Cappelin, B., Dutschmann, M., & Gestreau, C. (2009). Stimulation of the rat medullary raphe nuclei induces differential responses in respiratory muscle activity. Respiratory Physiology & Neurobiology, 165(2-3), 208-214. https://doi.org/10.1016/j.resp.2008.12.004.
Blazing, R. M., & Franks, K. M. (2020). Odor coding in piriform cortex: Mechanistic insights into distributed coding. Current Opinion in Neurobiology, 64, 96-102. https://doi.org/10.1016/j.conb.2020.03.001.
Burke, P. G. R., Abbott, S. B. G., McMullan, S., Goodchild, A. K., & Pilowsky, P. M. (2010). Somatostatin selectively ablates post-inspiratory activity after injection into the Bötzinger complex. Neuroscience, 167(2), 528-539. https://doi.org/10.1016/j.neuroscience.2010.01.065.
Butler, J. E. (2007). Drive to the human respiratory muscles. Respiratory Physiology & Neurobiology, 159(2), 115-126. https://doi.org/10.1016/j.resp.2007.06.006.
Caille, D., Vibert, J. F., & Hugelin, A. (1981). Apneusis and apnea after parabrachial or Kölliker-Fuse N. lesion; influence of wakefulness. Respiration Physiology, 45(1), 79-95. https://doi.org/10.1016/0034-5687(81)90051-7.
Carrive, P. (1993). The periaqueductal gray and defensive behavior: Functional representation and neuronal organization. Behavioural Brain Research, 58, 27-47. https://doi.org/10.1016/0166-4328(93)90088-8.
Carrive, P., Bandler, R., & Dampney, R. A. L. (1988). Anatomical evidence that hypertension associated with the defence reaction in the cat is mediated by a direct projection from a restricted portion of the midbrain periaqueductal grey to the subretrofacial nucleus of the medulla. Brain Research, 460(2), 339-345. https://doi.org/10.1016/0006-8993(88)90378-2.
Carrive, P., Leung, P., Harris, J., & Paxinos, G. (1997). Conditioned fear to context is associated with increased Fos expression in the caudal ventrolateral region of the midbrain periaqueductal gray. Neuroscience, 78(1), 165-177. https://doi.org/10.1016/S0306-4522(97)83047-3.
Chang, F. C. T. (1992). Modification of medullary respiratory-related discharge patterns by behaviors and states of arousal. Brain Research, 571(2), 281-292. https://doi.org/10.1016/0006-8993(92)90666-W.
Chapuis, J., Cohen, Y., He, X., Zhang, Z., Jin, S., Xu, F., & Wilson, D. A. (2013). Lateral entorhinal modulation of piriform cortical activity and fine odor discrimination. Journal of Neuroscience, 33(33), 13449-13459. https://doi.org/10.1523/JNEUROSCI.1387-13.2013.
Cobos Pallares, F. P., Bautista, T. G., Stanić, D., Egger, V., & Dutschmann, M. (2016). Brainstem-mediated sniffing and respiratory modulation during odor stimulation. Respiratory Physiology & Neurobiology, 233, 17-24. https://doi.org/10.1016/j.resp.2016.07.008.
Corfield, D. R., Murphy, K., & Guz, A. (1998). Does the motor cortical control of the diaphragm ‘bypass’ the brain stem respiratory centres in man? Respiration Physiology, 114(2), 109-117. https://doi.org/10.1016/S0034-5687(98)00083-8.
Dampney, R. A. (2015). Central mechanisms regulating coordinated cardiovascular and respiratory function during stress and arousal. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 309(5), R429-R443. https://doi.org/10.1152/ajpregu.00051.2015.
Dampney, R. A., Furlong, T. M., Horiuchi, J., & Iigaya, K. (2013). Role of dorsolateral periaqueductal grey in the coordinated regulation of cardiovascular and respiratory function. Autonomic Neuroscience, 175(1-2), 17-25. https://doi.org/10.1016/j.autneu.2012.12.008.
Davis, P. J., Zhang, S. P., Winkworth, A., & Bandler, R. (1996). Neural control of vocalization: Respiratory and emotional influences. Journal of Voice, 10(1), 23-38. https://doi.org/10.1016/S0892-1997(96)80016-6.
del Negro, C. A., Funk, G. D., & Feldman, J. L. (2018). Breathing matters. Nature Reviews Neuroscience, 19, 351-367. https://doi.org/10.1038/s41583-018-0003-6.
Depaulis, A., Bandler, R., & Vergnes, M. (1989). Characterization of pretentorial periaqueductal gray matter neurons mediating intraspecific defensive behaviors in the rat by microinjections of kainic acid. Brain Research, 486(1), 121-132. https://doi.org/10.1016/0006-8993(89)91284-5.
Deschênes, M., Moore, J., & Kleinfeld, D. (2012). Sniffing and whisking in rodents. Current Opinion in Neurobiology, 22, 243-250. https://doi.org/10.1016/j.conb.2011.11.013.
Dhingra, R. R., Dick, T. E., Furuya, W. I., Galán, R. F., & Dutschmann, M. (2020). Volumetric mapping of the functional neuroanatomy of the respiratory network in the perfused brainstem preparation of rats. The Journal of Physiology., 598, 2045-2046. https://doi.org/10.1113/JP279732.
Dhingra, R. R., Furuya, W. I., Bautista, T. G., Dick, T. E., Galán, R. F., & Dutschmann, M. (2019). Increasing local excitability of brainstem respiratory nuclei reveals a distributed network underlying respiratory motor pattern formation. Frontiers in Physiology, 10, 887. https://doi.org/10.3389/fphys.2019.00887.
Dhingra, R. R., Furuya, W. I., Galán, R. F., & Dutschmann, M. (2019). Excitation-inhibition balance regulates the patterning of spinal and cranial inspiratory motor outputs in rats in situ. Respiratory Physiology & Neurobiology, 266, 95-102. https://doi.org/10.1016/j.resp.2019.05.001.
Dick, T. E., Oku, Y., Romaniuk, J. R., & Cherniack, N. S. (1993). Interaction between central pattern generators for breathing and swallowing in the cat. The Journal of Physiology, 465(1), 715-730. https://doi.org/10.1113/jphysiol.1993.sp019702.
Dillingham, C. M., Jankowski, M. M., Chandra, R., Frost, B. E., & O'Mara, S. M. (2017). The claustrum: Considerations regarding its anatomy, functions and a programme for research. Brain and Neuroscience Advances, 1, 2398212817718962. https://doi.org/10.1177/2398212817718962.
Düsterhöft, F., Häusler, U., & Jürgens, U. (2004). Neuronal activity in the periaqueductal gray and bordering structures during vocal communication in the squirrel monkey. Neuroscience, 123(1), 53-60. https://doi.org/10.1016/j.neuroscience.2003.07.007.
Dutschmann, M., Bautista, T. G., Trevizan-Baú, P., Dhingra, R. R., & Furuya, W. I. (2020). The pontine Kölliker-Fuse nucleus gates facial, hypoglossal, and vagal upper airway related motor activity. Respiratory Physiology & Neurobiology, 284, 103563. https://doi.org/10.1016/j.resp.2020.103563.
Dutschmann, M., & Dick, T. E. (2012). Pontine mechanisms of respiratory control. Comprehensive Physiology, 2, 2443-2469. https://doi.org/10.1002/cphy.c100015.
Dutschmann, M., & Herbert, H. (2006). The Kölliker-Fuse nucleus gates the postinspiratory phase of the respiratory cycle to control inspiratory off-switch and upper airway resistance in rat. European Journal of Neuroscience, 24, 1071-1084. https://doi.org/10.1111/j.1460-9568.2006.04981.x.
Dutschmann, M., Jones, S. E., Subramanian, H. H., Stanić, D., & Bautista, T. G. (2014). The physiological significance of postinspiration in respiratory control. In Progress in brain research (Vol. 212, pp. 113-130). Elsevier. https://doi.org/10.1016/B978-0-444-63488-7.00007-0.
Dutschmann, M., & Paton, J. F. (2002). Inhibitory synaptic mechanisms regulating upper airway patency. Respiratory Physiology & Neurobiology, 131(1-2), 57-63. https://doi.org/10.1016/S1569-9048(02)00037-X.
Farmer, D. G., Bautista, T. G., Jones, S. E., Stanić, D., & Dutschmann, M. (2014). The midbrain periaqueductal grey has no role in the generation of the respiratory motor pattern, but provides command function for the modulation of respiratory activity. Respiratory Physiology & Neurobiology, 204, 14-20. https://doi.org/10.1016/j.resp.2014.07.011.
Faull, O. K., Subramanian, H. H., Ezra, M., & Pattinson, K. T. (2019). The midbrain periaqueductal gray as an integrative and interoceptive neural structure for breathing. Neuroscience & Biobehavioral Reviews, 98, 135-144. https://doi.org/10.1016/j.neubiorev.2018.12.020.
Feldman, J. L., & del Negro, C. A. (2006). Looking for inspiration: New perspectives on respiratory rhythm. Nature Reviews Neuroscience, 7, 232-241. https://doi.org/10.1038/nrn1871.
Finkelstein, D. I., Stanic, D., Parish, C. L., Tomas, D., Dickson, K., & Horne, M. K. (2000). Axonal sprouting following lesions of the rat substantia nigra. Neuroscience, 97, 99-112. https://doi.org/10.1016/s0306-4522(00)00009-9.
Floyd, N. S., Price, J. L., Ferry, A. T., Keay, K. A., & Bandler, R. (2000). Orbitomedial prefrontal cortical projections to distinct longitudinal columns of the periaqueductal gray in the rat. Journal of Comparative Neurology, 422(4), 556-578. https://doi.org/10.1002/1096-9861(20000710)422:4%3C556::AID-CNE6%3E3.0.CO;2-U.
Franklin, T. B. (2019). Recent advancements surrounding the role of the periaqueductal gray in predators and prey. Frontiers in Behavioral Neuroscience, 13, 60. https://doi.org/10.3389/fnbeh.2019.00060.
Fukushi, I., Yokota, S., & Okada, Y. (2019). The role of the hypothalamus in modulation of respiration. Respiratory Physiology & Neurobiology, 265, 172-179. https://doi.org/10.1016/j.resp.2018.07.003.
Gandevia, S. C., & Rothwell, J. C. (1987a). Knowledge of motor commands and the recruitment of human motoneurons. Brain, 110(5), 1117-1130. https://doi.org/10.1093/brain/110.5.1117.
Gandevia, S. C., & Rothwell, J. C. (1987b). Activation of the human diaphragm from the motor cortex. The Journal of Physiology, 384(1), 109-118. https://doi.org/10.1113/jphysiol.1987.sp016445.
Geerling, J. C., Shin, J. W., Chimenti, P. C., & Loewy, A. D. (2010). Paraventricular hypothalamic nucleus: Axonal projections to the brainstem. Journal of Comparative Neurology, 518(9), 1460-1499. https://doi.org/10.1002/cne.22283.
Grady, F., Peltekian, L., Iverson, G., & Geerling, J. C. (2020). DirectpParabrachial-cortical connectivity. Cerebral Cortex, 30, 4811-4833. https://doi.org/10.1093/cercor/bhaa072.
Hage, S. R., & Nieder, A. (2016). Dual neural network model for the evolution of speech and language. Trends in Neurosciences, 39(12), 813-829. https://doi.org/10.1016/j.tins.2016.10.006.
Harper, R. M., Frysinger, R. C., Trelease, R. B., & Marks, J. D. (1984). State-dependent alteration of respiratory cycle timing by stimulation of the central nucleus of the amygdala. Brain Research, 306(1-2), 1-8. https://doi.org/10.1016/0006-8993(84)90350-0.
Hermann, D. M., Luppi, P. H., Peyron, C., Hinckel, P., & Jouvet, M. (1997). Afferent projections to the rat nuclei raphe magnus, raphe pallidus and reticularis gigantocellularis pars α demonstrated by iontophoretic application of choleratoxin (subunit b). Journal of Chemical Neuroanatomy, 13, 1-21. https://doi.org/10.1016/S0891-0618(97)00019-7.
Hodges, M. R., & Richerson, G. B. (2010). The role of medullary serotonin (5-HT) neurons in respiratory control: Contributions to eupneic ventilation, CO2 chemoreception, and thermoregulation. Journal of Applied Physiology, 108(5), 1425-1432. https://doi.org/10.1152/japplphysiol.01270.2009.
Holstege, G. (1989). Anatomical study of the final common pathway for vocalization in the cat. Journal of Comparative Neurology, 284(2), 242-252. https://doi.org/10.1002/cne.902840208.
Holstege, G. (2014). The periaqueductal gray controls brainstem emotional motor systems including respiration. In Progress in brain research (Vol. 209, pp. 379-405). Elsevier. https://doi.org/10.1016/B978-0-444-63274-6.00020-5.
Holstege, G., & Subramanian, H. H. (2016). Two different motor systems are needed to generate human speech. Journal of Comparative Neurology, 524(8), 1558-1577. https://doi.org/10.1002/cne.23898.
Holtman, J. R., Dick, T. E., & Berger, A. J. (1986). Involvement of serotonin in the excitation of phrenic motoneurons evoked by stimulation of the raphe obscurus. Journal of Neuroscience, 6(4), 1185-1193. https://doi.org/10.1523/JNEUROSCI.06-04-01185.1986.
Homma, I., & Masaoka, Y. (2008). Breathing rhythms and emotions. Experimental Physiology, 93(9), 1011-1021. https://doi.org/10.1113/expphysiol.2008.042424.
Jean, A. (2001). Brain stem control of swallowing: Neuronal network and cellular mechanisms. Physiological Reviews, 81(2), 929-969. https://doi.org/10.1152/physrev.2001.81.2.929.
Jürgens, U. (1994). The role of the periaqueductal grey in vocal behaviour. Behavioural Brain Research, 62(2), 107-117. https://doi.org/10.1016/0166-4328(94)90017-5.
Jürgens, U. (2002). A study of the central control of vocalization using the squirrel monkey. Medical Engineering & Physics, 24(7-8), 473-477. https://doi.org/10.1016/S1350-4533(02)00051-6.
Jürgens, U. (2009). The neural control of vocalization in mammals: A review. Journal of Voice, 23, 1-10. https://doi.org/10.1016/j.jvoice.2007.07.005.
Jürgens, U., & Richter, K. (1986). Glutamate-induced vocalization in the squirrel monkey. Brain Research, 373(1-2), 349-358. https://doi.org/10.1016/0006-8993(86)90349-5.
Kataoka, N., Hioki, H., Kaneko, T., & Nakamura, K. (2014). Psychological stress activates a dorsomedial hypothalamus-medullary raphe circuit driving brown adipose tissue thermogenesis and hyperthermia. Cell Metabolism, 20(2), 346-358. https://doi.org/10.1016/j.cmet.2014.05.018.
Kleinfeld, D., Deschênes, M., Wang, F., & Moore, J. D. (2014). More than a rhythm of life: Breathing as a binder of orofacial sensation. Nature Neuroscience, 17(5), 647-651. https://doi.org/10.1038/nn.3693.
Laplagne, D. A. (2018). Interplay between mammalian ultrasonic vocalizations and respiration. In Handbook of behavioral neuroscience (Vol. 25, pp. 61-70). Elsevier. https://doi.org/10.1016/B978-0-12-809600-0.00006-8.
Larson, C. R. (1985). The midbrain periaqueductal gray: A brainstem structure involved in vocalization. Journal of Speech, Language, and Hearing Research, 28(2), 241-249. https://doi.org/10.1044/jshr.2802.241.
Leitner, F. C., Melzer, S., Lütcke, H., Pinna, R., Seeburg, P. H., Helmchen, F., & Monyer, H. (2016). Spatially segregated feedforward and feedback neurons support differential odor processing in the lateral entorhinal cortex. Nature Neuroscience, 19(7), 935-944. https://doi.org/10.1038/nn.4303.
Li, P., Janczewski, W. A., Yackle, K., Kam, K., Pagliardini, S., Krasnow, M. A., & Feldman, J. L. (2016). The peptidergic control circuit for sighing. Nature, 530(7590), 293-297. https://doi.org/10.1038/nature16964.
Li, P., Li, S. B., Wang, X., Phillips, C. D., Schwarz, L. A., Luo, L., de Lecea, L., & Krasnow, M. A. (2020). Brain circuit of claustrophobia-like behavior in mice identified by upstream tracing of sighing. Cell Reports, 31(11), 107779. https://doi.org/10.1016/j.celrep.2020.107779.
Lindsey, B. G., Arata, A., Morris, K. F., Hernandez, Y. M., & Shannon, R. (1998). Medullary raphe neurones and baroreceptor modulation of the respiratory motor pattern in the cat. The Journal of Physiology, 512(3), 863-882. https://doi.org/10.1111/j.1469-7793.1998.863bd.x.
Ludlow, C. L. (2015). Laryngeal reflexes: Physiology, technique and clinical use. Journal of Clinical Neurophysiology, 32(4), 284-293. https://doi.org/10.1097/WNP.0000000000000187.
Marchenko, V., Koizumi, H., Mosher, B., Koshiya, N., Tariq, M. F., Bezdudnaya, T. G., Zhang, R., Molkov, Y. I., Rybak, I. A., & Smith, J. C. (2016). Perturbations of respiratory rhythm and pattern by disrupting synaptic inhibition within pre-Bötzinger and Bötzinger complexes. ENeuro, 3(2), ENEURO.0011-ENEU16.2016. https://doi.org/10.1523/ENEURO.0011-16.2016.
Mazzone, S. B., Cole, L. J., Ando, A., Egan, G. F., & Farrell, M. J. (2011). Investigation of the neural control of cough and cough suppression in humans using functional brain imaging. Journal of Neuroscience, 31(8), 2948-2958. https://doi.org/10.1523/JNEUROSCI.4597-10.2011.
McElvain, L. E., Friedman, B., Karten, H. J., Svoboda, K., Wang, F., Deschênes, M., & Kleinfeld, D. (2018). Circuits in the rodent brainstem that control whisking in concert with other orofacial motor actions. Neuroscience, 368, 152-170. https://doi.org/10.1016/j.neuroscience.2017.08.034.
Moore, J. D., Deschênes, M., Furuta, T., Huber, D., Smear, M. C., Demers, M., & Kleinfeld, D. (2013). Hierarchy of orofacial rhythms revealed through whisking and breathing. Nature, 497(7448), 205-210. https://doi.org/10.1038/nature12076.
Moore, J. D., Kleinfeld, D., & Wang, F. (2014). How the brainstem controls orofacial behaviors comprised of rhythmic actions. Trends in Neurosciences, 37, 370-380. https://doi.org/10.1016/j.tins.2014.05.001.
Mörschel, M., & Dutschmann, M. (2009). Pontine respiratory activity involved in inspiratory/expiratory phase transition. Philosophical Transactions of the Royal Society B: Biological Sciences, 364(1529), 2517-2526. https://doi.org/10.1098/rstb.2009.0074.
Nonaka, S., Sakamoto, T., Katada, A., & Unno, T. (1999). Brain stem neural mechanisms for vocalization in decerebrate cats. Annals of Otology, Rhinology & Laryngology, 108(7_suppl), 15-24. https://doi.org/10.1177/00034894991080S703.
Onimaru, H., & Homma, I. (2007). Spontaneous oscillatory burst activity in the piriform-amygdala region and its relation to in vitro respiratory activity in newborn rats. Neuroscience, 144(1), 387-394. https://doi.org/10.1016/j.neuroscience.2006.09.033.
Orem, J., & Netick, A. (1986). Behavioral control of breathing in the cat. Brain Research, 366(1-2), 238-253. https://doi.org/10.1016/0006-8993(86)91301-6.
Paxinos, G., & Watson, C. (2007). The rat brain in stereotaxic coordinates. Academic Press.
Petersen, C. C. (2019). Sensorimotor processing in the rodent barrel cortex. Nature Reviews Neuroscience, 20(9), 533-546. https://doi.org/10.1038/s41583-019-0200-y.
Peyron, C., Tighe, D. K., van den Pol, A. N., de Lecea, L., Heller, H. C., Sutcliffe, J. G., & Kilduff, T. S. (1998). Neurons containing hypocretin (orexin) project to multiple neuronal systems. Journal of Neuroscience, 18(23), 9996-10015. https://doi.org/10.1523/JNEUROSCI.18-23-09996.1998.
Pouget, P., Allard, E., Poitou, T., Raux, M., Wattiez, N., & Similowski, T. (2018). Slower is higher: Threshold modulation of cortical activity in voluntary control of breathing initiation. Frontiers in Neuroscience, 12, 663. https://doi.org/10.3389/fnins.2018.00663.
Richter, D. W., Manzke, T., Wilken, B., & Ponimaskin, E. (2003). Serotonin receptors: Guardians of stable breathing. Trends in Molecular Medicine, 9(12), 542-548. https://doi.org/10.1016/j.molmed.2003.10.010.
Rikard-Bell, G. C., Bystrzycka, E. K., & Nail, B. S. (1985). Cells of origin of corticospinal projections to phrenic and thoracic respiratory motoneurones in the cat as shown by retrograde transport of HRP. Brain Research Bulletin, 14(1), 39-47. https://doi.org/10.1016/0361-9230(85)90175-3.
Ruggiero, D. A., Mraovitch, S., Granata, A. R., Anwar, M., & Reis, D. J. (1987). A role of insular cortex in cardiovascular function. Journal of Comparative Neurology, 257(2), 189-207. https://doi.org/10.1002/cne.902570206.
Saper, C. B. (1982). Convergence of autonomic and limbic connections in the insular cortex of the rat. Journal of Comparative Neurology, 210(2), 163-173. https://doi.org/10.1002/cne.902100207.
Sarkar, S., Zaretskaia, M. V., Zaretsky, D. V., Moreno, M., & DiMicco, J. A. (2007). Stress-and lipopolysaccharide-induced c-fos expression and nNOS in hypothalamic neurons projecting to medullary raphe in rats: A triple immunofluorescent labeling study. European Journal of Neuroscience, 26(8), 2228-2238. https://doi.org/10.1111/j.1460-9568.2007.05843.x.
Sato, F., Akhter, F., Haque, T., Kato, T., Takeda, R., Nagase, Y., Sessle, B. J., & 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, 9-27. https://doi.org/10.1016/j.neuroscience.2012.12.024.
Semba, K., & Egger, M. D. (1986). The facial “motor” nerve of the rat: Control of vibrissal movement and examination of motor and sensory components. Journal of Comparative Neurology, 247(2), 144-158. https://doi.org/10.1002/cne.902470203.
Sherwood, C. C., Hof, P. R., Holloway, R. L., Semendeferi, K., Gannon, P. J., Frahm, H. D., & Zilles, K. (2005). Evolution of the brainstem orofacial motor system in primates: A comparative study of trigeminal, facial, and hypoglossal nuclei. Journal of Human Evolution, 48, 45-84. https://doi.org/10.1016/j.jhevol.2004.10.003.
Smith, J. C., Abdala, A. P., Borgmann, A., Rybak, I. A., & Paton, J. F. (2013). Brainstem respiratory networks: Building blocks and microcircuits. Trends in Neurosciences, 36(3), 152-162. https://doi.org/10.1016/j.tins.2012.11.004.
Smith, J. C., Abdala, A. P. L., Koizumi, H., Rybak, I. A., & Paton, J. F. (2007). Spatial and functional architecture of the mammalian brain stem respiratory network: A hierarchy of three oscillatory mechanisms. Journal of Neurophysiology, 98, 3370-3387. https://doi.org/10.1152/jn.00985.2007.
Smith, J. C., Ellenberger, H. H., Ballanyi, K., Richter, D. W., & Feldman, J. L. (1991). Pre-Botzinger complex: A brainstem region that may generate respiratory rhythm in mammals. Science, 254, 726-729. https://doi.org/10.1126/science.1683005.
Stanic, D., Finkelstein, D. I., Bourke, D. W., Drago, J., & Horne, M. K. (2003). Timecourse of striatal re-innervation following lesions of the dopaminergic SNpc neurons of the rat. European Journal of Neuroscience, 18, 1175-1188. https://doi.org/10.1046/j.1460-9568.2003.02800.x.
Steinmetz, N. A., Zatka-Haas, P., Carandini, M., & Harris, K. D. (2019). Distributed coding of choice, action and engagement across the mouse brain. Nature, 576(7786), 266-273. https://doi.org/10.1038/s41586-019-1787-x.
Subramanian, H., Huang, Z. G., & Balnave, R. (2008). Responses of brainstem respiratory neurons to activation of midbrain periaqueductal gray in the rat. In Integration in respiratory control (pp. 377-381). Springer.
Subramanian, H. H., Balnave, R. J., & Holstege, G. (2008). The midbrain periaqueductal gray control of respiration. Journal of Neuroscience, 28(47), 12274-12283. https://doi.org/10.1523/JNEUROSCI.4168-08.2008.
Subramanian, H. H., & Holstege, G. (2009). The nucleus retroambiguus control of respiration. Journal of Neuroscience, 29(12), 3824-3832. https://doi.org/10.1523/JNEUROSCI.0607-09.2009.
Subramanian, H. H., & Holstege, G. (2014). The midbrain periaqueductal gray changes the eupneic respiratory rhythm into a breathing pattern necessary for survival of the individual and of the species. In Progress in brain research (Vol. 212, pp. 351-384). Elsevier. https://doi.org/10.1016/B978-0-444-63488-7.00017-3.
Tan, W., Pagliardini, S., Yang, P., Janczewski, W. A., & Feldman, J. L. (2010). Projections of preBötzinger complex neurons in adult rats. Journal of Comparative Neurology, 518(10), 1862-1878. https://doi.org/10.1002/cne.22308.
Trevizan-Baú, P., Furuya, W. I., Mazzone, S. B., Stanić, D., Dhingra, R. R., & Dutschmann, M. (2020). Reciprocal connectivity of the lateral and ventrolateral columns of the midbrain periaqueductal gray with core nuclei of ponto-medullary respiratory network in rat. Brain Research. https://doi.org/10.1101/2020.08.21.260422/.
Tupone, D., Madden, C. J., Cano, G., & Morrison, S. F. (2011). An orexinergic projection from perifornical hypothalamus to raphe pallidus increases rat brown adipose tissue thermogenesis. Journal of Neuroscience, 31(44), 15944-15955. https://doi.org/10.1523/JNEUROSCI.3909-11.2011.
Verdejo-Garcia, A., Clark, L., & Dunn, B. D. (2012). The role of interoception in addiction: A critical review. Neuroscience & Biobehavioral Reviews, 36(8), 1857-1869. https://doi.org/10.1016/j.neubiorev.2012.05.007.
Wang, W., Fung, M. L., & St John, W. M. (1993). Pontile regulation of ventilatory activity in the adult rat. Journal of Applied Physiology, 74(6), 2801-2811. https://doi.org/10.1152/jappl.1993.74.6.2801.
Woolsey, T. A., & van der Loos, H. (1970). The structural organization of layer IV in the somatosensory region (SI) of mouse cerebral cortex: The description of a cortical field composed of discrete cytoarchitectonic units. Brain Research, 17(2), 205-242. https://doi.org/10.1016/0006-8993(70)90079-X.
Yang, C. F., & Feldman, J. L. (2018). Efferent projections of excitatory and inhibitory preBötzinger complex neurons. Journal of Comparative Neurology, 526(8), 1389-1402. https://doi.org/10.1002/cne.24415.
Yang, C. F., Kim, E. J., Callaway, E. M., & Feldman, J. L. (2020). Monosynaptic projections to excitatory and inhibitory preBötzinger complex neurons. Frontiers in Neuroanatomy, 14, 58. https://doi.org/10.3389/fnana.2020.00058.
Yasui, Y., Breder, C. D., Safer, C. B., & Cechetto, D. F. (1991). Autonomic responses and efferent pathways from the insular cortex in the rat. Journal of Comparative Neurology, 303(3), 355-374. https://doi.org/10.1002/cne.903030303.
Zald, D. H., & Pardo, J. V. (1999). The functional neuroanatomy of voluntary swallowing. Annals of Neurology: Official Journal of the American Neurological Association and the Child Neurology Society, 46(3), 281-286. https://doi.org/10.1002/1531-8249(199909)46:3<281::AID-ANA2>3.0.CO;2-L.
Zhang, S. P., Bandler, R., & Davis, P. J. (1995). Brain stem integration of vocalization: Role of the nucleus retroambigualis. Journal of Neurophysiology, 74(6), 2500-2512. https://doi.org/10.1152/jn.1995.74.6.2500.
Zhang, S. P., Davis, P. J., Bandler, R., & Carrive, P. (1994). Brain stem integration of vocalization: Role of the midbrain periaqueductal gray. Journal of Neurophysiology, 72(3), 1337-1356. https://doi.org/10.1152/jn.1994.72.3.1337.