Inhibitory actions of melanin-concentrating hormone in the lateral septum.
electrophysiology
hypothalamus
melanin‐concentrating hormone
neuroanatomy
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
14 Jun 2024
14 Jun 2024
Historique:
received:
11
04
2023
accepted:
21
05
2024
medline:
14
6
2024
pubmed:
14
6
2024
entrez:
14
6
2024
Statut:
aheadofprint
Résumé
Melanin-concentrating hormone (MCH) neurons can co-express several neuropeptides or neurotransmitters and send widespread projections throughout the brain. Notably, there is a dense cluster of nerve terminals from MCH neurons in the lateral septum (LS) that innervate LS cells by glutamate release. The LS is also a key region integrating stress- and anxiety-like behaviours, which are also emerging roles of MCH neurons. However, it is not known if or where the MCH peptide acts within the LS. We analysed the projections from MCH neurons in male and female mice anteroposteriorly throughout the LS and found spatial overlap between the distribution pattern of MCH-immunoreactive (MCH-ir) fibres with MCH receptor Mchr1 mRNA hybridization or MCHR1-ir cells. This overlap was most prominent along the ventral and lateral border of the rostral part of the LS (LSr). Most MCHR1-labelled LS neurons lay adjacent to passing MCH-ir fibres, but some MCH-ir varicosities directly contacted the soma or cilium of MCHR1-labelled LS neurons. We thus performed whole-cell patch-clamp recordings from MCHR1-rich LSr regions to determine if and how LS cells respond to MCH. Bath application of MCH to acute brain slices activated a bicuculline-sensitive chloride current that directly hyperpolarized LS cells. This MCH-mediated hyperpolarization was blocked by calphostin C, which suggested that the inhibitory actions of MCH were mediated by protein kinase C-dependent activation of GABA
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Canadian Government | Natural Sciences and Engineering Research Council of Canada (NSERC)
ID : RGPIN-2024-04133
Organisme : Canadian Government | Natural Sciences and Engineering Research Council of Canada (NSERC)
ID : RGPIN-2017-06272
Organisme : Canadian Government | Natural Sciences and Engineering Research Council of Canada (NSERC)
ID : Postgraduate Doctoral Scholarship
Organisme : Canadian Government | Natural Sciences and Engineering Research Council of Canada (NSERC)
ID : Canadian Graduate Master's Scholarship
Organisme : Canadian Government | Canadian Institutes of Health Research (CIHR)
ID : PJT-175156
Organisme : Ontario Ministry of Colleges and Universities
ID : Ontario Graduate Scholarship
Informations de copyright
© 2024 The Author(s). The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Adamantidis, A., & de Lecea, L. (2009). A role for melanin‐concentrating hormone in learning and memory. Peptides, 30(11), 2066–2070.
Adamantidis, A., Thomas, E., Foidart, A., Tyhon, A., Coumans, B., Minet, A., Tirelli, E., Seutin, V., Grisar, T., & Lakaye, B. (2005). Disrupting the melanin‐concentrating hormone receptor 1 in mice leads to cognitive deficits and alterations of NMDA receptor function. European Journal of Neuroscience, 21(10), 2837–2844.
Anthony, T. E., Dee, N., Bernard, A., Lerchner, W., Heintz, N., & Anderson, D. J. (2014). Control of stress‐induced persistent anxiety by an extra‐amygdala septohypothalamic circuit. Cell, 156(3), 522–536.
Bächner, D., Kreienkamp, H. J., Weise, C., Buck, F., & Richter, D. (1999). Identification of melanin concentrating hormone (MCH) as the natural ligand for the orphan somatostatin‐like receptor 1 (SLC‐1). FEBS Letters, 457(3), 522–524.
Bakshi, V. P., Newman, S. M., Smith‐roe, S., Jochman, K. A., & Kalin, N. H. (2007). Stimulation of lateral septum CRF 2 receptors promotes anorexia and stress‐like behaviors : Functional homology to CRF 1 receptors in basolateral amygdala. Journal of Neuroscience, 27(39), 10568–10577.
Bang, J. Y., Zhao, J., Rahman, M., St‐Cyr, S., McGowan, P. O., & Kim, J. C. (2022). Hippocampus‐anterior hypothalamic circuit modulates stress‐induced endocrine and behavioral response. Frontiers in Neural Circuits, 16, 894722.
Barson, J. R., Morganstern, I., & Leibowitz, S. F. (2013). Complementary roles of orexin and melanin‐concentrating hormone in feeding behavior. International Journal of Endocrinology, 2013, 983964.
Beekly, B. G., Frankel, W. C., Berg, T., Allen, S. J., Garcia‐Galiano, D., Vanini, G., & Elias, C. F. (2020). Dissociated Pmch and Cre expression in lactating Pmch‐Cre BAC transgenic mice. Frontiers in Neuroanatomy, 14, 60.
Berbari, N. F., Johnson, A. D., Lewis, J. S., Askwith, C. C., & Mykytyn, K. (2008). Identification of ciliary localization sequences within the third intracellular loop of G protein‐coupled receptors. Molecular Biology of the Cell, 19(4), 1540–1547.
Bittencourt, J. C., Presse, F., Arias, C., Peto, C., Vaughan, J., Nahon, J.‐L., Vale, W., & Sawchenko, P. E. (1992). The melanin‐concentrating hormone system of the rat brain: An immuno‐ and hybridization histochemical characterization. Journal of Comparative Neurology, 319(2), 218–245.
Bono, B. S., Ly, N. K. K., Miller, P. A., Williams‐Ikhenoba, J., Dumiaty, Y., & Chee, M. J. (2022). Spatial distribution of beta‐klotho mRNA in the mouse hypothalamus, hippocampal region, subiculum, and amygdala. Journal of Comparative Neurology, 530(10), 1634–1657.
Bouyer, K., & Simerly, R. B. (2013). Neonatal leptin exposure specifies innervation of presympathetic hypothalamic neurons and improves the metabolic status of leptin‐deficient mice. Journal of Neuroscience, 33(2), 840–851.
Broberger, C. (1999). Hypothalamic cocaine‐ and amphetamine‐regulated transcript (CART) neurons: Histochemical relationship to thyrotropin‐releasing hormone, melanin‐concentrating hormone, orexin/hypocretin and neuropeptide Y. Brain Research, 848(1–2), 101–113.
Broberger, C., de Lecea, L., Sutcliffe, J. G., Ho¨kfelt, T., & Ho¨kfelt, H. (1998). Hypocretin/orexin‐and melanin‐concentrating hormone‐expressing cells form distinct populations in the rodent lateral hypothalamus: Relationship to the neuropeptide Y and agouti gene‐related protein systems. Journal of Comparative Neurology, 402(4), 460–474.
Calderwood, M. T., Tseng, A., & Glenn Stanley, B. (2020). Lateral septum mu opioid receptors in stimulation of feeding. Brain Research, 1734, 146648.
Carette, B., Poulain, P., & Beauvillain, J. C. (2001). Noradrenaline modulates GABA‐mediated synaptic transmission in neurones of the mediolateral part of the guinea pig lateral septum via local circuits. Neuroscience Research, 39(1), 71–77.
Chee, M. J. S., Arrigoni, E., & Maratos‐Flier, E. (2015). Melanin‐concentrating hormone neurons release glutamate for feedforward inhibition of the lateral septum. Journal of Neuroscience, 35(8), 3644–3651.
Chee, M. J. S., Pissios, P., & Maratos‐Flier, E. (2013). Neurochemical characterization of neurons expressing melanin‐concentrating hormone receptor 1 in the mouse hypothalamus. Journal of Comparative Neurology, 521(10), 2208–2234.
Chen, P., Lin, D., Giesler, J., & Li, C. (2011). Identification of urocortin 3 afferent projection to the ventromedial nucleus of the hypothalamus in rat brain. Journal of Comparative Neurology, 519(10), 2023–2042.
Croizier, S., Franchi‐Bernard, G., Colard, C., Poncet, F., la Roche, A., & Risold, P. Y. (2010). A comparative analysis shows morphofunctional differences between the rat and mouse melanin‐concentrating hormone systems. PLoS ONE, 5(11), e15471.
Dilsiz, P., Aklan, I., Sayar Atasoy, N., Yavuz, Y., Filiz, G., Koksalar, F., Ates, T., Oncul, M., Coban, I., Ates Oz, E., Cebecioglu, U., Alp, M., Yilmaz, B., & Atasoy, D. (2020). MCH neuron activity is sufficient for reward and reinforces feeding. Neuroendocrinology, 110(3–4), 258–270.
Diniz, G. B., Battagello, D. S., Klein, M. O., Bono, B. S. M., Ferreira, J. G. P., Motta‐Teixeira, L. C., Duarte, J. C. G., Presse, F., Nahon, J. L., Adamantidis, A., Chee, M. J., Sita, L. V., & Bittencourt, J. C. (2020). Ciliary melanin‐concentrating hormone receptor 1 (MCHR1) is widely distributed in the murine CNS in a sex‐independent manner. Journal of Neuroscience Research, 98(10), 2045–2071.
Dong, H. W. (2008). The Allen reference atlas: A digital color brain atlas of the C57BL/6J male mouse. John Wiley & Sons.
Drugan, R., Skolnick, P., Paul, S., & Crawley, J. N. (1986). Low doses of muscimol produce anticonflict actions in the lateral septum of the rat. Neuropharmacology, 25(2), 203–205.
Du Sert, N. P., Hurst, V., Ahluwalia, A., Alam, S., Avey, M. T., Baker, M., Browne, W. J., Clark, A., Cuthill, I. C., Dirnagl, U., Emerson, M., Garner, P., Holgate, S. T., Howells, D. W., Karp, N. A., Lazic, S. E., Lidster, K., MacCallum, C. J., Macloed, M., … Würbel, H. (2020). The ARRIVE guidelines 2.0: Updated guidelines for reporting animal research. Experimental Physiology, 105(9), 1459–1466.
Ebner, K., Muigg, P., Singewald, G., & Singewald, N. (2008). Substance P in stress and anxiety NK‐1 receptor antagonism interacts with key brain areas of the stress circuitry. Annals of the New York Academy of Sciences, 1144, 61–73.
Elias, C. F., Saper, C. B., Maratos‐Flier, E., Tritos, N. A., Lee, C., Kelly, J., Tatro, J. B., Huffman, G. E., Ollmann, M. M., Barsh, G. S., Sakurai, T., Yanagisawa, M., & Elmquist, J. K. (1998). Chemically defined projections linking the mediobasal hypothalamus and the lateral hypothalamic area. Journal of Comparative Neurology, 402(4), 442–459.
Ferreira, J., Bittencourt, J., & Adamantidis, A. (2017). Melanin‐concentrating hormone and sleep. Current Opinion in Neurobiology, 44, 152–158.
Gabriella, I., Tseng, A., Sanchez, K. O., Shah, H., Stanley, B. G., Gabriella, I., Tseng, A., Sanchez, K. O., Shah, H., & Stanley, B. G. (2022). Stimulation of GABA receptors in the lateral septum rapidly elicits food intake and mediates natural feeding. Brain Sciences, 12(7), 848.
Gallagher, J. P., & Hasuo, H. (1989). Bicuculline‐ and phaclofen‐sensitive components of N‐methyl‐D‐aspartate‐induced hyperpolarizations in rat dorsolateral septal nucleus neurones. The Journal of Physiology, 418, 367–377.
Gallagher, J. P., Zheng, F., Hasuo, H., & Shinnick‐Gallagher, P. (1995). Activities of neurons within the rat dorsolateral septal nucleus (DLSN). Progress in Neurobiology, 45(5), 373–395.
Gao, X. (2009). Electrophysiological effects of MCH on neurons in the hypothalamus. Peptides, 30(11), 2025–2030.
Gavioli, E. C., Canteras, N. S., & de Lima, T. C. M. (1999). Anxiogenic‐like effect induced by substance P injected into the lateral septal nucleus. Neuroreport, 10(16), 3399–3403.
Gavioli, E. C., Canteras, N. S., & De Lima, T. C. M. (2002). The role of lateral septal NK1 receptors in mediating anxiogenic effects induced by intracerebroventricular injection of substance P. Behavioural Brain Research, 134(1–2), 411–415.
Georgescu, D., Sears, R. M., Hommel, J. D., Barrot, M., Bolan, C. A., Marsh, D. J., Bednarek, M. A., Bibb, J. A., Maratos‐flier, E., Nestler, E. J., & Dileone, R. J. (2005). The hypothalamic neuropeptide melanin‐concentrating hormone acts in the nucleus accumbens to modulate feeding behavior and forced‐swim performance. Journal of Neuroscience, 25(11), 2933–2940.
Greer, P. L., Bear, D. M., Lassance, J.‐M., Bloom, M. L., Tsukahara, T., Pashkovski, S. L., Masuda, F. K., Nowlan, A. C., Kirchner, R., Hoekstra, H. E., & Datta, S. R. (2016). A family of non‐GPCR chemosensors defines an alternative logic for mammalian olfaction. Cell, 165(7), 1734–1748.
Grundy, D. (2015). Principles and standards for reporting animal experiments in The Journal of Physiology and Experimental Physiology. Journal of Physics, 593(12), 2547–2549.
Harthoorn, L., Sañé, A., Nethe, M., & van Heerikhuize, J. (2005). Multi‐transcriptional profiling of melanin‐concentrating hormone and orexin‐containing neurons. Cellular and Molecular Neurobiology, 25(8), 1209–1223.
Hassani, O. K., Lee, M. G., & Jones, B. E. (2009). Melanin‐concentrating hormone neurons discharge in a reciprocal manner to orexin neurons across the sleep‐wake cycle. Proceedings of the National Academy of Sciences, USA, 106(7), 2418–2422.
Hawes, B., Kil, E., Green, B., O'Neill, K., Fried, S., & Graziano, M. (2000). The melanin‐concentrating hormone receptor couples to multiple G proteins to activate diverse intracellular signaling pathways. Endocrinology, 141(12), 4524–4532.
He, S., Shao, L.‐R., Rittase, W. B., & Bausch, S. B. (2012). Increased Kv1 channel expression may contribute to decreased sIPSC frequency following chronic inhibition of NR2B‐containing NMDAR. Neuropsychopharmacology, 37(6), 1338–1356.
Heldt, S. A., & Ressler, K. J. (2007). Forebrain and midbrain distribution of major benzodiazepine‐sensitive GABAA receptor subunits in the adult C57 mouse as assessed with in situ hybridization. Neuroscience, 150(2), 370–385.
Hervieu, G., Cluderay, J., Harrison, D., Meakin, J., Maycox, P., Nasir, S., & Leslie, R. (2000). The distribution of the mRNA and protein products of the melanin‐concentrating hormone (MCH) receptor gene, slc‐1, in the central nervous system of the rat. European Journal of Neuroscience, 12(4), 1194–1216.
Hill, J., Duckworth, M., Murdock, P., Rennie, G., Sabido‐David, C., Ames, R. S., Szekeres, P., Wilson, S., Bergsma, D. J., Gloger, I. S., Levy, D. S., Chambers, J. K., & Muir, A. I. (2001). Molecular cloning and functional characterization of MCH2, a novel human MCH receptor. Journal of Biological Chemistry, 276(23), 20125–20129.
Hörtnagl, H., Tasan, R. O., Wieselthaler, A., Kirchmair, E., Sieghart, W., & Sperk, G. (2013). Patterns of mRNA and protein expression for 12 GABAA receptor subunits in the mouse brain. Neuroscience, 236, 345–372.
Jego, S., Glasgow, S. D., Herrera, C. G., Ekstrand, M., Reed, S. J., Boyce, R., Friedman, J., Burdakov, D., & Adamantidis, A. R. (2013). Optogenetic identification of a rapid eye movement sleep modulatory circuit in the hypothalamus. Nature Neuroscience, 16(11), 1637–1643.
Kela, J., Salmi, P., Rimondini‐Giorgini, R., Heilig, M., & Wahlestedt, C. (2003). Behavioural analysis of melanin‐concentrating hormone in rats: evidence for orexigenic and anxiolytic properties. Regulatory Peptides, 114(2–3), 109–114.
Kim, T.‐K., & Han, P.‐L. (2016). Physical exercise counteracts stress‐induced upregulation of melanin‐concentrating hormone in the brain and stress‐induced persisting anxiety‐like behaviors. Experimental Neurobiology, 25(4), 163–173.
Kokkotou, E., Jeon, J. Y., Wang, X., Marino, F. E., Carlson, M., Trombly, D. J., Maratos‐flier, E., Jeon, J. Y., Wang, X., Marino, F. E., Carlson, M., Trombly, D. J., & Mice, E. M. (2005). Mice with MCH ablation resist diet‐induced obesity through strain‐specific mechanisms. American Journal of Physiology‐Regulatory, Integrative and Comparative Physiology, 289(1), R117–R124.
Kovacs, E. G., Szalay, F., & Halasy, K. (2005). Fasting‐induced changes of neuropeptide immunoreactivity in the lateral septum of male rats. Acta Biologica Hungarica, 56(3–4), 185–197.
Krimer, L. S., Jakab, R. L., & Goldman‐Rakic, P. S. (1997). Quantitative three‐dimensional analysis of the catecholaminergic innervation of identified neurons in the macaque prefrontal cortex. Journal of Neuroscience, 17(19), 7450–7461.
Lambe, E. K., Krimer, L. S., & Goldman‐Rakic, P. S. (2000). Differential postnatal development of catecholamine and serotonin inputs to identified neurons in prefrontal cortex of rhesus monkey. Journal of Neuroscience, 20(23), 8780–8787.
Lee, V., & Maguire, J. (2014). The impact of tonic GABAA receptor‐mediated inhibition on neuronal excitability varies across brain region and cell type. Frontiers in Neural Circuits, 8, 3.
Lembo, P. M. C., Grazzini, E., Cao, J., Hubatsch, D. A., Pelletier, M., Hoffert, C., St‐Onge, S., Pou, C., Labrecque, J., Groblewski, T., O'Donnell, D., Payza, K., Ahmad, S., & Walker, P. (1999). The receptor for the orexigenic peptide melanin‐concentrating hormone is a G‐protein‐coupled receptor. Nature Cell Biology, 1(5), 267–271.
Le Merrer, J., Cagniard, B., & Cazala, P. (2006). Modulation of anxiety by mu‐opioid receptors of the lateral septal region in mice. Pharmacology Biochemistry and Behavior, 83(3), 465–479.
Lin, Y. F., Angelotti, T. P., Dudek, E. M., Browning, M. D., & Macdonald, R. L. (1996). Enhancement of recombinant α1β1γ2L γ‐aminobutyric acid(A) receptor whole‐cell currents by protein kinase C is mediated through phosphorylation of both β1 and γ2L subunits. Molecular Pharmacology, 50(1), 185–195.
Lin, Y. F., Browning, M. D., Dudek, E. M., & Macdonald, R. L. (1994). Protein kinase C enhances recombinant bovine α1β1γ2L GABAA receptor whole‐cell currents expressed in L929 fibroblasts. Neuron, 13(6), 1421–1431.
Lipo, E., Asrat, S., Huo, W., Sol, A., Fraser, C. S., & Isberg, R. R. (2022). 5’ untranslated mRNA regions allow bypass of host cell translation inhibition by Legionella pneumophila. Infection and Immunity, 90(11), e0017922.
Liu, J.‐J., Tsien, R. W., & Pang, Z. P. (2022). Hypothalamic melanin‐concentrating hormone regulates hippocampus‐dorsolateral septum activity. Nature Neuroscience, 25(1), 61–71.
Ludwig, D., Tritos, N., Mastaitis, J., Kulkarni, R., Kokkotou, E., Elmquist, J., Lowell, B., Flier, J., & Maratos‐Flier, E. (2001). Melanin‐concentrating hormone overexpression in transgenic mice leads to obesity and insulin resistance. Journal of Clinical Investigation, 107(3), 379–386.
Mansour, A., Fox, C. A., Burke, S., Meng, F., Thompson, R. C., Akil, H., & Watson, S. J. (1994). Mu, delta, and kappa opioid receptor mRNA expression in the Rat CNS: An in situ hybridization study. Journal of Comparative Neurology, 350(3), 412–438.
Masiulis, S., Desai, R., Uchański, T., Serna Martin, I., Laverty, D., Karia, D., Malinauskas, T., Zivanov, J., Pardon, E., Kotecha, A., Steyaert, J., Miller, K. W., & Aricescu, A. R. (2019). GABAA receptor signalling mechanisms revealed by structural pharmacology. Nature, 565(7740), 454–459.
Mickelsen, L., Bolisetty, M., Chimileski, B., Fujita, A., Beltrami, E., Costanzo, J., Naparstek, J., Robson, P., & Jackson, A. (2019). Single‐cell transcriptomic analysis of the lateral hypothalamic area reveals molecularly distinct populations of inhibitory and excitatory neurons. Nature Neuroscience, 22(4), 642–656.
Mickelsen, L. E., Kolling, F. W., IV, Chimileski, B. R., Fujita, A., Norris, C., Chen, K., Nelson, C. E., & Jackson, A. C. (2017). Neurochemical heterogeneity among lateral hypothalamic hypocretin/orexin and melanin‐concentrating hormone neurons identified through single‐cell gene expression analysis. eNeuro, 4(5), 13–17.
Miller, P. A., Williams‐Ikhenoba, J. G., Sankhe, A. S., Hoffe, B. H., & Chee, M. J. (2024). Neuroanatomical, electrophysiological, and morphological characterization of melanin‐concentrating hormone cells coexpressing cocaine‐ and amphetamine‐regulated transcript. Journal of Comparative Neurology, 532(2), e25588.
Mogi, K., Funabashi, T., Mitsushima, D., Hagiwara, H., & Kimura, F. (2005). Sex difference in the response of melanin‐concentrating hormone neurons in the lateral hypothalamic area to glucose, as revealed by the expression of phosphorylated cyclic adenosine 3,5‐monophosphate response element‐binding protein. Endocrinology, 146(8), 3325–3333.
Monzon, M., de Souza, M., Izquierdo, L., Izquierdo, I., Barros, D., & de Barioglio, S. (1999). Melanin‐concentrating hormone (MCH) modifies memory retention in rats. Peptides, 20(12), 1517–1519.
Mu, M.‐D., Geng, H.‐Y., Rong, K.‐L., Peng, R.‐C., Wang, S.‐T., Geng, L.‐T., Qian, Z.‐M., Yung, W.‐H., & Ke, Y. (2020). A limbic circuitry involved in emotional stress‐induced grooming. Nature Communications, 11(1), 2261.
Mul, J. D., la Fleur, S. E., Toonen, P. W., Afrasiab‐Middelman, A., Binnekade, R., Schetters, D., Verheij, M. M. M., Sears, R. M., Homberg, J. R., Schoffelmeer, A. N. M., Adan, R. A. H., DiLeone, R. J., de Vries, T. J., & Cuppen, E. (2011). Chronic loss of melanin‐concentrating hormone affects motivational aspects of feeding in the rat. PLoS ONE, 6(5), e19600.
Mystkowski, P., Seeley, R. J., Hahn, T. M., Baskin, D. G., Havel, P. J., Matsumoto, A. M., Wilkinson, C. W., Peacock‐Kinzig, K., Blake, K. A., & Schwartz, M. W. (2000). Hypothalamic melanin‐concentrating hormone and estrogen‐induced weight loss. Journal of Neuroscience, 20(22), 8637–8642.
Negishi, K., Payant, M. A., Schumacker, K. S., Wittmann, G., Butler, R. M., Lechan, R. M., Steinbusch, H. W. M., Khan, A. M., & Chee, M. J. (2020). Distributions of hypothalamic neuron populations coexpressing tyrosine hydroxylase and the vesicular GABA transporter in the mouse. Journal of Comparative Neurology, 528(11), 1833–1855.
Noble, E., Hahn, J., Konanur, V., Hsu, T., Page, S., Cortella, A., Liu, C., Song, M., Suarez, A., Szujewski, C., Rider, D., Clarke, J., Darvas, M., Appleyard, S., & Kanoski, S. (2018). Control of feeding behavior by cerebral ventricular volume transmission of melanin‐concentrating hormone. Cell metabolism, 28(1), 55–68. e7.
Noguchi, T., Makino, S., Shinahara, M., Nishiyama, M., Hashimoto, K., & Terada, Y. (2013). Effects of gold thioglucose treatment on central corticotrophin‐releasing hormone systems in mice. Journal of Neuroendocrinology, 25(4), 340–349.
Onteniente, B., Geffard, M., Campistron, G., & Calas, A. (1987). An ultrastructural study of GABA‐immunoreactive neurons and terminals in the septum of the rat. Journal of Neuroscience, 7(1), 48–54.
Parfitt, G. M., Nguyen, R., Yoon Bang, J., Aqrabawi, A. J., Tran, M. M., Seo, K., Richards, B. A., & Kim, J. C. (2017). Bidirectional control of anxiety‐related behaviors in mice: Role of inputs arising from the ventral hippocampus to the lateral septum and medial prefrontal cortex. Neuropsychopharmacology, 42(8), 1715–1728.
Pedemonte, M., Barrenechea, C., Nuñez, A., Gambini, J. P., & García‐Austt, E. (1998). Membrane and circuit properties of lateral septum neurons: Relationships with hippocampal rhythms. Brain Research, 800(1), 145–153.
Pesold, C., & Treit, D. (1996). The neuroanatomical specificity of the anxiolytic effects of intra‐septal infusions of midazolam. Brain Research, 710(1–2), 161–168.
Phelan, K. D., Hasuo, H., Twery, M. J., & Gallagher, J. P. (1989). Projection neurons in the rat dorsolateral septal nucleus possess recurrent axon collaterals. Neuroscience Letters, 97(3), 259–265.
Pissios, P., Bradley, R., & Maratos‐Flier, E. (2006). Expanding the scales: The multiple roles of MCH in regulating energy balance and other biological functions. Endocrine Reviews, 27(6), 606–620.
Pissios, P., Trombly, D. J., Tzameli, I., & Maratos‐Flier, E. (2003). Melanin‐concentrating hormone receptor 1 activates extracellular signal‐regulated kinase and synergizes with Gs‐coupled pathways. Endocrinology, 144(8), 3514–3523.
Poisbeau, P., Cheney, M. C., Browning, M. D., & Mody, I. (1999). Modulation of synaptic GABA(A) receptor function by PKA and PKC in adult hippocampal neurons. Journal of Neuroscience, 19(2), 674–683.
Qu, D., Ludwig, D., Gammeltoft, S., Piper, M., Pelleymounter, M., Cullen, M., Mathes, W., Przypek, R., Kanarek, R., & Maratos‐Flier, E. (1996). A role for melanin‐concentrating hormone in the central regulation of feeding behaviour. Nature, 380(6571), 243–247.
Rao, Y., Lu, M., Ge, F., Marsh, D. J., Qian, S., Wang, A. H., Picciotto, M. R., & Gao, X. B. (2008). Regulation of synaptic efficacy in hypocretin/orexin‐containing neurons by melanin concentrating hormone in the lateral hypothalamus. Journal of Neuroscience, 28(37), 9101–9110.
Risold, P. Y., & Swanson, L. W. (1997a). Connections of the rat lateral septal complex. Brain Research Brain Research Reviews, 24(2–3), 115–195.
Risold, P. Y., & Swanson, L. W. (1997b). Chemoarchitecture of the rat lateral septal nucleus. Brain Research Brain Research Reviews, 24(2–3), 91–113.
Rondini, T. A., de Crudis Rodrigues, B., de Oliveira, A. P., Bittencourt, J. C., & Elias, C. F. (2007). Melanin‐concentrating hormone is expressed in the laterodorsal tegmental nucleus only in female rats. Brain Research Bulletin, 74(1–3), 21–28.
Rossi, M., Choi, S. J., O'Shea, D., Miyoshi, T., Ghatei, M. A., & Bloom, S. R. (1997). Melanin‐concentrating hormone acutely stimulates feeding, but chronic administration has no effect on body weight. Endocrinology, 138(1), 351–355.
Ruiz‐Viroga, V., Urbanavicius, J., Torterolo, P., & Lagos, P. (2021). In vivo uptake of a fluorescent conjugate of melanin‐concentrating hormone in the rat brain. Journal of Chemical Neuroanatomy, 114, 101959.
Saito, Y., Cheng, M., Leslie, F. M., & Civelli, O. (2001). Expression of the melanin‐concentrating hormone (MCH) receptor mRNA in the rat brain. Journal of Comparative Neurology, 435(1), 26–40.
Saito, Y., Nothacker, H. P., Wang, Z., Lin, S. H. S., Leslie, F., & Civelli, O. (1999). Molecular characterization of the melanin‐concentrating‐hormone receptor. Nature, 400(6741), 265–269.
Sears, R. M., Liu, R. J., Narayanan, N. S., Sharf, R., Yeckel, M. F., Laubach, M., Aghajanian, G. K., & DiLeone, R. J. (2010). Regulation of nucleus accumbens activity by the hypothalamic neuropeptide melanin‐concentrating hormone. Journal of Neuroscience, 30(24), 8263–8273.
Sheehan, T. P., Chambers, R. A., & Russell, D. S. (2004). Regulation of affect by the lateral septum : Implications for neuropsychiatry. Brain Research Brain Research Reviews, 46(1), 71–117.
Shimada, M., Tritos, N. A., Lowell, B. B., Flier, J. S., & Maratos‐Flier, E. (1998). Mice lacking melanin‐concentrating hormone are hypophagic and lean. Nature, 396(6712), 670–674.
Skofitsch, G., Jacobowitz, D. M., & Zamir, N. (1985). Immunohistochemical localization of a melanin concentrating hormone‐like peptide in the rat brain. Brain Research Bulletin, 15(6), 635–649.
Spencer, C. D., Miller, P. A., Williams‐Ikhenoba, J. G., Nikolova, R. G., & Chee, M. J. (2024). Regulation of the mouse ventral tegmental area by melanin‐concentrating hormone. Journal of Neuroscience, e0790232024.
Staiger, J. F., & Nürnberger, F. (1991). The efferent connections of the lateral septal nucleus in the guinea pig: Intrinsic connectivity of the septum and projections to other telencephalic areas. Cell and Tissue Research, 264(3), 415–426.
Stengel, A., & Taché, Y. (2014). CRF and urocortin peptides as modulators of energy balance and feeding behavior during stress. Frontiers in Neuroscience, 8, 52.
Swanson, L. W., & Cowan, W. M. (1977). An autoradiographic study of the organization of the efferet connections of the hippocampal formation in the rat. Journal of Comparative Neurology, 172(1), 49–84.
Takase, K., Kikuchi, K., Tsuneoka, Y., Oda, S., & Kuroda, M. (2014). Meta‐analysis of melanin‐concentrating hormone signaling‐deficient mice on behavioral and metabolic phenotypes. PLoS ONE, 9(6), e99961.
Tan, C. P., Sano, H., Iwaasa, H., Pan, J., Sailer, A. W., Hreniuk, D. L., Feighner, S. D., Palyha, O. C., Pong, S. S., Figueroa, D. J., Austin, C. P., Jiang, M. M., Yu, H., Ito, J., Ito, M., Ito, M., Guan, X. M., MacNeil, D. J., Kanatani, A., … Howard, A. D. (2002). Melanin‐concentrating hormone receptor subtypes 1 and 2: Species‐specific gene expression. Genomics, 79(6), 785–792.
Teixeira, P. D. S., Wasinski, F., Lima, L. B., Frazão, R., Bittencourt, J. C., & Donato, J. (2020). Regulation and neurochemical identity of melanin‐concentrating hormone neurones in the preoptic area of lactating mice. Journal of Neuroendocrinology, 32(2), e12818.
Terrill, S. J., Subramanian, K. S., Lan, R., Liu, C. M., Cortella, A. M., Noble, E. E., & Kanoski, S. E. (2020). Nucleus accumbens melanin‐concentrating hormone signaling promotes feeding in a sex‐specific manner HHS Public Access. Neuropharmacology, 178, 108270.
Valeyev, A. Y., Hackman, J. C., Holohean, A. M., Wood, P. M., Katz, J. L., & Davidoff, R. A. (1999). GABA‐induced Cl‐ current in cultured embryonic human dorsal root ganglion neurons. Journal of Neurophysiology, 82(1), 1–9.
Van Pett, K., Viau, V., Bittencourt, J., Chan, R., Li, H., Arias, C., Prins, G., Perrin, M., Vale, W., & Sawchenko, P. (2000). Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. Journal of Comparative Neurology, 428(2), 191–212.
Verret, L., Goutagny, R., Fort, P., Cagnon, L., Salvert, D., Léger, L., Boissard, R., Salin, P., Peyron, C., & Luppi, P.‐H. (2003). A role of melanin‐concentrating hormone producing neurons in the central regulation of paradoxical sleep. BMC Neuroscience [Electronic Resource], 4, 19.
Wang, C., & Kotz, C. (2002). Urocortin in the lateral septal area modulates feeding induced by orexin A in the lateral hypothalamus. American Journal of Physiology‐Regulatory, Integrative and Comparative Physiology, 283(2), R358–R367.
Wollman, L. B., Levine, R. B., & Fregosi, R. F. (2018). Developmental nicotine exposure alters glycinergic neurotransmission to hypoglossal motoneurons in neonatal rats. Journal of Neurophysiology, 120(3), 1135–1142.
Wu, M., Dumalska, I., Morozova, E., van den Pol, A., & Alreja, M. (2009). Melanin‐concentrating hormone directly inhibits GnRH neurons and blocks kisspeptin activation, linking energy balance to reproduction. Proceedings of the National Academy of Sciences, USA, 106(40), 17217–17222.
Xu, Y., Lu, Y., Cassidy, R., Mangieri, L., Zhu, C., Huang, X., Jiang, Z., Justice, N., Xu, Y., Arenkiel, B., & Tong, Q. (2019). Identification of a neurocircuit underlying regulation of feeding by stress‐related emotional responses. Nature Communications, 10(1), 3446.
Zhao, C., Eisinger, B., & Gammie, S. C. (2013). Characterization of GABAergic neurons in the mouse lateral septum: A double fluorescence in situ hybridization and immunohistochemical study using tyramide signal amplification. PLoS ONE, 8(8), e73750.
Zheng, H., Patterson, L. M., Morrison, C., Banfield, B. W., Randall, J. A., Browning, K. N., Travagli, R. A., & Berthoud, H. R. (2005). Melanin concentrating hormone innervation of caudal brainstem areas involved in gastrointestinal functions and energy balance. Neuroscience, 135(2), 611–625.