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Erschienen in: Brain Structure and Function 9/2016

18.02.2016 | Original Article

Microarray analysis of transcripts with elevated expressions in the rat medial or lateral habenula suggest fast GABAergic excitation in the medial habenula and habenular involvement in the regulation of feeding and energy balance

verfasst von: Franziska Wagner, René Bernard, Christian Derst, Leon French, Rüdiger W. Veh

Erschienen in: Brain Structure and Function | Ausgabe 9/2016

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Abstract

In vertebrates the “anti-reward-system” mainly is represented by the habenula and its medial (MHb) and especially lateral (LHb) complexes. Considerable knowledge has accumulated concerning subnuclear structures and connectivities of MHb and LHb subnuclei. The present investigation aimed to obtain novel information, whether MHb or LHb or their subnuclei display field-characteristic gene products, which may shed light on biological functions of these areas. Unfortunately this was not the case. Microarray analysis of mRNAs in microdissected habenular and thalamic control areas yielded expression values of 17,745 RNAs representing protein-coding genes, to which annotated gene names could be assigned. High relative values of genes with known expression in MHb, LHb or thalamus in the corresponding areas indicated a high precision of the microdissection procedure. Note that the present report emphasizes differences between and not absolute expression values in the selected regions. The present investigation disclosed that the LHb genetically is much closer related to the thalamus as compared to the MHb. The results presented here focuse on gene transcripts related to major transmitter systems, catecholamines and neuropeptides. Quite surprisingly, our data indicate potentially inhibitory effects of acetylcholine and glutamate in the habenula. In addition, the absence of the K-Cl co-transporter 2 supports a largely excitatory role of GABAergic transmission especially in the MHb. Furthermore, several G-protein related receptors (Gpr83, Gpr139, Gpr149, Gpr151, Gpr158) and many neuropeptides related to feeding are differentially expressed in the habenular region, indicating that its involvement in the regulation of food consumption and energy expenditure may have been underestimated so far.
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Literatur
Zurück zum Zitat Aizawa H, Kobayashi M, Tanaka SC, Fukai T, Okamoto H (2012) Molecular characterization of the subnuclei in rat habenula. J Comp Neurol 520:4051–4066PubMedCrossRef Aizawa H, Kobayashi M, Tanaka SC, Fukai T, Okamoto H (2012) Molecular characterization of the subnuclei in rat habenula. J Comp Neurol 520:4051–4066PubMedCrossRef
Zurück zum Zitat Andres KH, von Düring M, Veh RW (1999) Subnuclear organization of the rat habenular complexes. J Comp Neurol 407:130–150PubMedCrossRef Andres KH, von Düring M, Veh RW (1999) Subnuclear organization of the rat habenular complexes. J Comp Neurol 407:130–150PubMedCrossRef
Zurück zum Zitat Araki M, McGeer PL, Kimura H (1988) The efferent projections of the rat lateral habenular nucleus revealed by the PHA-L anterograde tracing method. Brain Res 441:319–330PubMedCrossRef Araki M, McGeer PL, Kimura H (1988) The efferent projections of the rat lateral habenular nucleus revealed by the PHA-L anterograde tracing method. Brain Res 441:319–330PubMedCrossRef
Zurück zum Zitat Bear MF, Connors BW, Paradiso MA (2007) Neuroscience: exploring the brain. Williams and Wilkins, Baltimore Bear MF, Connors BW, Paradiso MA (2007) Neuroscience: exploring the brain. Williams and Wilkins, Baltimore
Zurück zum Zitat Begriche K, Girardet C, McDonald P, Butler AA (2013) Melanocortin-3 receptors and metabolic homeostasis. Progr Mol Biol Transl Sci 114:109–146CrossRef Begriche K, Girardet C, McDonald P, Butler AA (2013) Melanocortin-3 receptors and metabolic homeostasis. Progr Mol Biol Transl Sci 114:109–146CrossRef
Zurück zum Zitat Bernard R, Veh RW (2012) Individual neurons in the rat lateral habenular complex project mostly to the dopaminergic ventral tegmental area or to the serotonergic raphe nuclei. J Comp Neurol 520:2545–2558PubMedCrossRef Bernard R, Veh RW (2012) Individual neurons in the rat lateral habenular complex project mostly to the dopaminergic ventral tegmental area or to the serotonergic raphe nuclei. J Comp Neurol 520:2545–2558PubMedCrossRef
Zurück zum Zitat Berthold M, Collin M, Sejlitz T, Meister B, Lind P (2003) Cloning of a novel orphan G protein-coupled receptor (GPCR-2037): in situ hybridization reveals high mRNA expression in rat brain restricted to neurons of the habenular complex. Mol Brain Res 120:22–29PubMedCrossRef Berthold M, Collin M, Sejlitz T, Meister B, Lind P (2003) Cloning of a novel orphan G protein-coupled receptor (GPCR-2037): in situ hybridization reveals high mRNA expression in rat brain restricted to neurons of the habenular complex. Mol Brain Res 120:22–29PubMedCrossRef
Zurück zum Zitat Bjursell M, Ahnmark A, Bohlooly-Y M, William-Olsson L, Rhedin M, Peng XR, Ploj K, Gerdin AK, Arnerup G, Elmgren A, Berg AL, Oscarsson J, Linden D (2007) Opposing effects of adiponectin receptors 1 and 2 on energy metabolism. Diabetes 56:583–593PubMedCrossRef Bjursell M, Ahnmark A, Bohlooly-Y M, William-Olsson L, Rhedin M, Peng XR, Ploj K, Gerdin AK, Arnerup G, Elmgren A, Berg AL, Oscarsson J, Linden D (2007) Opposing effects of adiponectin receptors 1 and 2 on energy metabolism. Diabetes 56:583–593PubMedCrossRef
Zurück zum Zitat Boschert U, Amara DA, Segu L, Hen R (1994) The mouse 5-hydroxytryptamine(1B) receptor is localized predominantly on axon terminals. Neuroscience 58:167–182PubMedCrossRef Boschert U, Amara DA, Segu L, Hen R (1994) The mouse 5-hydroxytryptamine(1B) receptor is localized predominantly on axon terminals. Neuroscience 58:167–182PubMedCrossRef
Zurück zum Zitat Brinschwitz K, Dittgen A, Madai VI, Lommel R, Geisler S, Veh RW (2010) Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 168:463–476PubMedCrossRef Brinschwitz K, Dittgen A, Madai VI, Lommel R, Geisler S, Veh RW (2010) Glutamatergic axons from the lateral habenula mainly terminate on GABAergic neurons of the ventral midbrain. Neuroscience 168:463–476PubMedCrossRef
Zurück zum Zitat Broms J, Antolin-Fontes B, Tingström A, Ibañez-Tallon I (2015) Conserved expression of the GPR151 receptor in habenular axonal projections of vertebrates. J Comp Neurol 523:359–380PubMedCrossRef Broms J, Antolin-Fontes B, Tingström A, Ibañez-Tallon I (2015) Conserved expression of the GPR151 receptor in habenular axonal projections of vertebrates. J Comp Neurol 523:359–380PubMedCrossRef
Zurück zum Zitat Brown AA, Jensen J, Nikolova YS, Djurovic S, Agartz I, Server A, Ferrell RE, Manuck SB, Mattingsdal M, Melle I, Hariri AR, Frigessi A, Andreassen OA (2012) Genetic variants affecting the neural processing of human facial expressions: evidence using a genome-wide functional imaging approach. Transl Psychiatry 2:e143PubMedPubMedCentralCrossRef Brown AA, Jensen J, Nikolova YS, Djurovic S, Agartz I, Server A, Ferrell RE, Manuck SB, Mattingsdal M, Melle I, Hariri AR, Frigessi A, Andreassen OA (2012) Genetic variants affecting the neural processing of human facial expressions: evidence using a genome-wide functional imaging approach. Transl Psychiatry 2:e143PubMedPubMedCentralCrossRef
Zurück zum Zitat Canela L, Luján R, Lluís C, Burgueño J, Mallol J, Canela EI, Franco R, Ciruela F (2007) The neuronal Ca2+-binding protein 2 (NECAB2) interacts with the adenosine A2A receptor and modulates the cell surface expression and function of the receptor. Mol Cell Neurosci 36:1–12PubMedCrossRef Canela L, Luján R, Lluís C, Burgueño J, Mallol J, Canela EI, Franco R, Ciruela F (2007) The neuronal Ca2+-binding protein 2 (NECAB2) interacts with the adenosine A2A receptor and modulates the cell surface expression and function of the receptor. Mol Cell Neurosci 36:1–12PubMedCrossRef
Zurück zum Zitat Capogna M, Pearce RA (2011) GABAA, slow: causes and consequences. Trends Neurosci 34:101–112PubMedCrossRef Capogna M, Pearce RA (2011) GABAA, slow: causes and consequences. Trends Neurosci 34:101–112PubMedCrossRef
Zurück zum Zitat Carter MS, Krause JE (1990) Structure, expression, and some regulatory mechanisms of the rat preprotachykinin gene encoding substance P, neurokinin A, neuropeptide K, and neuropeptide Y. J Neurosci 70:2203–2214 Carter MS, Krause JE (1990) Structure, expression, and some regulatory mechanisms of the rat preprotachykinin gene encoding substance P, neurokinin A, neuropeptide K, and neuropeptide Y. J Neurosci 70:2203–2214
Zurück zum Zitat Chamma I, Chevy Q, Poncer JC, Lévi S (2012) Role of the neuronal K-Cl co-transporter KCC2 in inhibitory and excitatory neurotransmission. Front Cell Neurosci 6, article 5:1 Chamma I, Chevy Q, Poncer JC, Lévi S (2012) Role of the neuronal K-Cl co-transporter KCC2 in inhibitory and excitatory neurotransmission. Front Cell Neurosci 6, article 5:1
Zurück zum Zitat Chastrette N, Pfaff DW, Gibbs RB (1991) Effects of daytime and nighttime stress on Fos-like immunoreactivity in the paraventricular nucleus of the hypothalamus, the habenula, and the posterior paraventricular nucleus of the thalamus. Brain Res 563:339–344PubMedCrossRef Chastrette N, Pfaff DW, Gibbs RB (1991) Effects of daytime and nighttime stress on Fos-like immunoreactivity in the paraventricular nucleus of the hypothalamus, the habenula, and the posterior paraventricular nucleus of the thalamus. Brain Res 563:339–344PubMedCrossRef
Zurück zum Zitat Christoph GR, Leonzio RJ, Wilcox KS (1986) Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmentum area of the rat. J Neurosci 6:613–619PubMed Christoph GR, Leonzio RJ, Wilcox KS (1986) Stimulation of the lateral habenula inhibits dopamine-containing neurons in the substantia nigra and ventral tegmentum area of the rat. J Neurosci 6:613–619PubMed
Zurück zum Zitat De Jong TR, Measor KT, Chauke M, Harris BN, Saltzman W (2010) Brief pup exposure induces Fos-expession in the lateral habenula and serotonergic caudal dorsal raphe nucleus of paternally experienced male california mice (Peromyscus californicus). Neuroscience 169:1094–1104PubMedCrossRef De Jong TR, Measor KT, Chauke M, Harris BN, Saltzman W (2010) Brief pup exposure induces Fos-expession in the lateral habenula and serotonergic caudal dorsal raphe nucleus of paternally experienced male california mice (Peromyscus californicus). Neuroscience 169:1094–1104PubMedCrossRef
Zurück zum Zitat Gagnon D, Parent M (2014) Distribution of VGLUT3 in highly collateralized axons from the rat dorsal raphe nucleus as revealed by single-neuron reconstructions. PLoS One 9(e87709):1–12 Gagnon D, Parent M (2014) Distribution of VGLUT3 in highly collateralized axons from the rat dorsal raphe nucleus as revealed by single-neuron reconstructions. PLoS One 9(e87709):1–12
Zurück zum Zitat Gardiner JV, Beale KE, Roy D, Boughton CK, Bataveljic A, Campbell DC, Bewick GA, Patel NA, Patterson M, Leavy EM, Ghatei MA, Bloom SR, Dhillo WS (2010) Cerebellin1 is a novel orexigenic peptide. Diabetes Obes Metab 12:883–890PubMedCrossRef Gardiner JV, Beale KE, Roy D, Boughton CK, Bataveljic A, Campbell DC, Bewick GA, Patel NA, Patterson M, Leavy EM, Ghatei MA, Bloom SR, Dhillo WS (2010) Cerebellin1 is a novel orexigenic peptide. Diabetes Obes Metab 12:883–890PubMedCrossRef
Zurück zum Zitat Geisler S, Heilmann H, Veh RW (2002) An optimized method for simultaneous demonstration of neurons and myelinated fiber tracts for delineation of individual trunco- and palliothalamic nuclei in the mammalian brain. Histochem Cell Biol 117:69–79PubMedCrossRef Geisler S, Heilmann H, Veh RW (2002) An optimized method for simultaneous demonstration of neurons and myelinated fiber tracts for delineation of individual trunco- and palliothalamic nuclei in the mammalian brain. Histochem Cell Biol 117:69–79PubMedCrossRef
Zurück zum Zitat Geisler S, Andres KH, Veh RW (2003) Morphologic and cytochemical criteria for the identification and delineation of individual subnuclei within the lateral habenular complex of the rat. J Comp Neurol 458:78–97PubMedCrossRef Geisler S, Andres KH, Veh RW (2003) Morphologic and cytochemical criteria for the identification and delineation of individual subnuclei within the lateral habenular complex of the rat. J Comp Neurol 458:78–97PubMedCrossRef
Zurück zum Zitat Gerstein MB, Bruce C, Rozowsky JS, Zheng D, Du J, Korbel JO, Emanuelsson O, Zhang ZD, Weissman S, Snyder M (2007) What is a gene, post-ENCODE? History and updated definition. Genome Res 17:669–681PubMedCrossRef Gerstein MB, Bruce C, Rozowsky JS, Zheng D, Du J, Korbel JO, Emanuelsson O, Zhang ZD, Weissman S, Snyder M (2007) What is a gene, post-ENCODE? History and updated definition. Genome Res 17:669–681PubMedCrossRef
Zurück zum Zitat Goncalves L, Sego C, Metzger M (2012) Differential projections from the lateral habenula to the rostromedial tegmental nucleus and ventral tegmental area in the rat. J Comp Neurol 520:1278–1300PubMedCrossRef Goncalves L, Sego C, Metzger M (2012) Differential projections from the lateral habenula to the rostromedial tegmental nucleus and ventral tegmental area in the rat. J Comp Neurol 520:1278–1300PubMedCrossRef
Zurück zum Zitat Good CH, Wang H, Chen YH, Mejias-Aponte CA, Hoffman AF, Lupica CR (2013) Dopamine D4 receptor excitation of lateral habenula neurons via multiple cellular mechanisms. J Neurosci 43:16853–16864CrossRef Good CH, Wang H, Chen YH, Mejias-Aponte CA, Hoffman AF, Lupica CR (2013) Dopamine D4 receptor excitation of lateral habenula neurons via multiple cellular mechanisms. J Neurosci 43:16853–16864CrossRef
Zurück zum Zitat Görlich A, Antolin-Fontes B, Ables JL, Frahm S, Slimak MA, Dougherty JD, Ibañez-Tallon I (2013) Reexposure to nicotine during withdrawal increases the pacemaking activity of cholinergic habenular neurons. Proc Nat Acad Sci USA 110:17077–17082PubMedPubMedCentralCrossRef Görlich A, Antolin-Fontes B, Ables JL, Frahm S, Slimak MA, Dougherty JD, Ibañez-Tallon I (2013) Reexposure to nicotine during withdrawal increases the pacemaking activity of cholinergic habenular neurons. Proc Nat Acad Sci USA 110:17077–17082PubMedPubMedCentralCrossRef
Zurück zum Zitat Görtzen A (1993) Neurotensin-Immunreaktivität im Habenularkomplex der Ratte. Ruhr-Universität, Bochum, GFR, p 68 Görtzen A (1993) Neurotensin-Immunreaktivität im Habenularkomplex der Ratte. Ruhr-Universität, Bochum, GFR, p 68
Zurück zum Zitat Gras C, Herzog E, Bellenchi GC, Bernard B, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442–5451PubMed Gras C, Herzog E, Bellenchi GC, Bernard B, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442–5451PubMed
Zurück zum Zitat Gruber C, Kahl A, Lebenheim L, Kowski A, Dittgen A, Veh RW (2007) Dopaminergic projections from the VTA substantially contribute to the mesohabenular pathway in the rat. Neurosci Lett 427:165–170PubMedCrossRef Gruber C, Kahl A, Lebenheim L, Kowski A, Dittgen A, Veh RW (2007) Dopaminergic projections from the VTA substantially contribute to the mesohabenular pathway in the rat. Neurosci Lett 427:165–170PubMedCrossRef
Zurück zum Zitat Gundlach AL, Knobe KE (1992) Distribution of preproatrial natriuretic peptide mRNA in rat brain detected by in situ hybridization of DNA oligonucleotides: enrichment in hypothalamic and limbic regions. J Neurochem 59:758–761PubMedCrossRef Gundlach AL, Knobe KE (1992) Distribution of preproatrial natriuretic peptide mRNA in rat brain detected by in situ hybridization of DNA oligonucleotides: enrichment in hypothalamic and limbic regions. J Neurochem 59:758–761PubMedCrossRef
Zurück zum Zitat Herkenham M, Nauta WJH (1977) Afferent connections of the habenular nuclei in the rat: a horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173:123–146PubMedCrossRef Herkenham M, Nauta WJH (1977) Afferent connections of the habenular nuclei in the rat: a horseradish peroxidase study, with a note on the fiber-of-passage problem. J Comp Neurol 173:123–146PubMedCrossRef
Zurück zum Zitat Herkenham M, Nauta WJH (1979) Efferent connections of the habenular nuclei in the rat. J Comp Neurol 18:19–48CrossRef Herkenham M, Nauta WJH (1979) Efferent connections of the habenular nuclei in the rat. J Comp Neurol 18:19–48CrossRef
Zurück zum Zitat Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S (2004) Localization of vGluT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:983–1002PubMedCrossRef Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S (2004) Localization of vGluT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:983–1002PubMedCrossRef
Zurück zum Zitat Hsu YWA, Tempest L, Quina LA, Wei AD, Zeng H, Turner EE (2013) Medial habenula output circuit mediated by a5 nicotinic receptor-expressing GABAergic neurons in the interpeduncular nucleus. J Neurosci 33:18022–18035PubMedPubMedCentralCrossRef Hsu YWA, Tempest L, Quina LA, Wei AD, Zeng H, Turner EE (2013) Medial habenula output circuit mediated by a5 nicotinic receptor-expressing GABAergic neurons in the interpeduncular nucleus. J Neurosci 33:18022–18035PubMedPubMedCentralCrossRef
Zurück zum Zitat Hwang E-K, Chung J-M (2014) 5HT1B receptor-mediated pre-synaptic depression of excitatory inputs to the rat lateral habenula. Neuropharmacology 81:153–165PubMedCrossRef Hwang E-K, Chung J-M (2014) 5HT1B receptor-mediated pre-synaptic depression of excitatory inputs to the rat lateral habenula. Neuropharmacology 81:153–165PubMedCrossRef
Zurück zum Zitat Ignatov A, Hermans-Borgmeyer I, Schaller HC (2004) Cloning and characterization of a novel G-protein-coupled receptor with homology to galanin receptors. Neuropharmacology 46:1114–1120PubMedCrossRef Ignatov A, Hermans-Borgmeyer I, Schaller HC (2004) Cloning and characterization of a novel G-protein-coupled receptor with homology to galanin receptors. Neuropharmacology 46:1114–1120PubMedCrossRef
Zurück zum Zitat Isberg V, Andersen KB, Bisig C, Dietz GPH, Bräuner-Osborne H, Gloriam DE (2014) Computer-aided discovery of aromatic l-α-amino acids as agonists of the orphan G protein-coupled receptor GPR139. J Chem Inf Model 54:1553–1557PubMedCrossRef Isberg V, Andersen KB, Bisig C, Dietz GPH, Bräuner-Osborne H, Gloriam DE (2014) Computer-aided discovery of aromatic l-α-amino acids as agonists of the orphan G protein-coupled receptor GPR139. J Chem Inf Model 54:1553–1557PubMedCrossRef
Zurück zum Zitat Ji H, Shepard PD (2007) Lateral habenula stimulation inhibits rat midbrain dopamine neurons through a GABA-A receptor-mediated mechanism. J Neurosci 27:6923–6930PubMedCrossRef Ji H, Shepard PD (2007) Lateral habenula stimulation inhibits rat midbrain dopamine neurons through a GABA-A receptor-mediated mechanism. J Neurosci 27:6923–6930PubMedCrossRef
Zurück zum Zitat Kasprzyk A (2011) BioMart: driving a paradigm change in biological data management. Database bar049:1–3 Kasprzyk A (2011) BioMart: driving a paradigm change in biological data management. Database bar049:1–3
Zurück zum Zitat Katoh Y, Takemori H, Horike N, Doi J, Muraoka M, Min L, Okamoto M (2004) Salt-inducible kinase (SIK) isoforms: their involvement in steroidogenesis and adipogenesis. Mol Cell Endocrinol 217:109–112PubMedCrossRef Katoh Y, Takemori H, Horike N, Doi J, Muraoka M, Min L, Okamoto M (2004) Salt-inducible kinase (SIK) isoforms: their involvement in steroidogenesis and adipogenesis. Mol Cell Endocrinol 217:109–112PubMedCrossRef
Zurück zum Zitat Kobayashi Y, Sano Y, Vannoni E, Goto H, Suzuki H, Oba A, Kawasaki H, Kanba S, Lipp H-P, Murphy NP, Wolfer DP, Itohara S (2013) Genetic dissection of medial habenula –interpeduncular nucleus pathway function in mice. Front Behav Neursci 7:1–20 Kobayashi Y, Sano Y, Vannoni E, Goto H, Suzuki H, Oba A, Kawasaki H, Kanba S, Lipp H-P, Murphy NP, Wolfer DP, Itohara S (2013) Genetic dissection of medial habenula –interpeduncular nucleus pathway function in mice. Front Behav Neursci 7:1–20
Zurück zum Zitat Kowski AB, Geisler S, Krauss M, Veh RW (2008) Differential projections from subfields in the lateral preoptic area to the lateral habenular complex of the rat. J Comp Neurol 507:1465–1478PubMedCrossRef Kowski AB, Geisler S, Krauss M, Veh RW (2008) Differential projections from subfields in the lateral preoptic area to the lateral habenular complex of the rat. J Comp Neurol 507:1465–1478PubMedCrossRef
Zurück zum Zitat Kowski AB, Veh RW, Weiss T (2009) Dopaminergic activation excites rat lateral habenular neurons in vivo. Neuroscience 161:1154–1165PubMedCrossRef Kowski AB, Veh RW, Weiss T (2009) Dopaminergic activation excites rat lateral habenular neurons in vivo. Neuroscience 161:1154–1165PubMedCrossRef
Zurück zum Zitat Kringelbach ML, Berridge KC (2010) The neuroscience of happiness and pleasure. Soc Res N Y 77:659–678 Kringelbach ML, Berridge KC (2010) The neuroscience of happiness and pleasure. Soc Res N Y 77:659–678
Zurück zum Zitat Kumar U (2012) Immunohistochemical distribution of somatostatin and somatostatin receptor subtypes (SSTR1–5) in hypothalamus of ApoD knockout mice brain. J Mol Neurosci 48:684–695PubMedCrossRef Kumar U (2012) Immunohistochemical distribution of somatostatin and somatostatin receptor subtypes (SSTR1–5) in hypothalamus of ApoD knockout mice brain. J Mol Neurosci 48:684–695PubMedCrossRef
Zurück zum Zitat Lateef DM, Abreu-Vieira G, Xiao C, Reitman ML (2014) Regulation of body temperature and brown adipose tissue thermogenesis by bombesin receptor subtype-3. Am J Physiol Endocrinol Metab 306:E681–E687PubMedPubMedCentralCrossRef Lateef DM, Abreu-Vieira G, Xiao C, Reitman ML (2014) Regulation of body temperature and brown adipose tissue thermogenesis by bombesin receptor subtype-3. Am J Physiol Endocrinol Metab 306:E681–E687PubMedPubMedCentralCrossRef
Zurück zum Zitat Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176PubMedCrossRef Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, Desaki AL, Desta T, Diep E, Dolbeare TA, Donelan MJ, Dong HW, Dougherty JG, Duncan BJ, Ebbert AJ, Eichele G, Estin LK, Faber C, Facer BA, Fields R, Fischer SR, Fliss TP, Frensley C, Gates SN, Glattfelder KJ, Halverson KR, Hart MR, Hohmann JG, Howell MP, Jeung DP, Johnson RA, Karr PT, Kawal R, Kidney JM, Knapik RH (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:168–176PubMedCrossRef
Zurück zum Zitat Leinninger GM, Jo YH, Leshan RL, Louis GW, Yang H, Barrera JG, Wilson H, Opland DM, Faouzi M, Gong Y, Jones JC, Rhodes CJ, Chua S Jr, Diano S, Horvath TL, Seeley RJ, Becker JB, Münzberg H, Myers MG Jr (2011) Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab 14:313–323PubMedPubMedCentralCrossRef Leinninger GM, Jo YH, Leshan RL, Louis GW, Yang H, Barrera JG, Wilson H, Opland DM, Faouzi M, Gong Y, Jones JC, Rhodes CJ, Chua S Jr, Diano S, Horvath TL, Seeley RJ, Becker JB, Münzberg H, Myers MG Jr (2011) Leptin action via neurotensin neurons controls orexin, the mesolimbic dopamine system and energy balance. Cell Metab 14:313–323PubMedPubMedCentralCrossRef
Zurück zum Zitat Lv S-Y, Yang Y-J, Chen Q (2013) Regulation of feeding behavior, gestroinntestinal function and fluid homestasis by apelin. Peptides 44:87–92PubMedCrossRef Lv S-Y, Yang Y-J, Chen Q (2013) Regulation of feeding behavior, gestroinntestinal function and fluid homestasis by apelin. Peptides 44:87–92PubMedCrossRef
Zurück zum Zitat Madai VI, Poller WC, Peters D, Berger J, Paliege K, Bernard R, Veh RW, Laube G (2012) Synaptic localisation of agmatinase in rat cerebral cortex revealed by virtual pre-embedding. Amino Acids 43:1399–1403PubMedCrossRef Madai VI, Poller WC, Peters D, Berger J, Paliege K, Bernard R, Veh RW, Laube G (2012) Synaptic localisation of agmatinase in rat cerebral cortex revealed by virtual pre-embedding. Amino Acids 43:1399–1403PubMedCrossRef
Zurück zum Zitat Matsuda K, Azuma M, Maruyama K, Shioda S (2013) Neuroendocrine control of feeding behavior and psychomotor activity by pituitary adenylate cyclase-activating polypeptide (PACAP) in vertebrates. Obes Res Clin Pract 7:e1–e7PubMedCrossRef Matsuda K, Azuma M, Maruyama K, Shioda S (2013) Neuroendocrine control of feeding behavior and psychomotor activity by pituitary adenylate cyclase-activating polypeptide (PACAP) in vertebrates. Obes Res Clin Pract 7:e1–e7PubMedCrossRef
Zurück zum Zitat Matsumoto M, Hikosaka O (2007) Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447:1111–1115PubMedCrossRef Matsumoto M, Hikosaka O (2007) Lateral habenula as a source of negative reward signals in dopamine neurons. Nature 447:1111–1115PubMedCrossRef
Zurück zum Zitat Meye FJ, Adan RAH (2014) Feelings about food: the ventral tegmental area in food reward and emotional eating. Trends Pharmacol Sci 35:31–40PubMedCrossRef Meye FJ, Adan RAH (2014) Feelings about food: the ventral tegmental area in food reward and emotional eating. Trends Pharmacol Sci 35:31–40PubMedCrossRef
Zurück zum Zitat Molnár G, Faragó N, Kocsis AK, Rózsa M, Lovas S, Boldog E, Báldi R, Csajbók E, Gardi J, Puskás LG, Tamás G (2014) GABAergic neurogliaform cells represent local sources of insulin in the cerebral cortex. J Neurosci 34:1133–1137PubMedCrossRef Molnár G, Faragó N, Kocsis AK, Rózsa M, Lovas S, Boldog E, Báldi R, Csajbók E, Gardi J, Puskás LG, Tamás G (2014) GABAergic neurogliaform cells represent local sources of insulin in the cerebral cortex. J Neurosci 34:1133–1137PubMedCrossRef
Zurück zum Zitat Müller A, Kleinau G, Piechowski CL, Müller TD, Finan B, Pratzka J, Grüters A, Krude H, Tschöp M, Biebermann H (2013) G-protein coupled receptor 83 (GPR83) signaling determined by constitutive and Zinc(II)-induced activity. PLoS One 8(e53347):1–9 Müller A, Kleinau G, Piechowski CL, Müller TD, Finan B, Pratzka J, Grüters A, Krude H, Tschöp M, Biebermann H (2013) G-protein coupled receptor 83 (GPR83) signaling determined by constitutive and Zinc(II)-induced activity. PLoS One 8(e53347):1–9
Zurück zum Zitat Ohishi H, Shigemoto R, Nakanishi S, Mizuno N (1993) Distribution of the messenger RNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an insitu hybridization study. J Comp Neurol 335(2):252–266PubMedCrossRef Ohishi H, Shigemoto R, Nakanishi S, Mizuno N (1993) Distribution of the messenger RNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an insitu hybridization study. J Comp Neurol 335(2):252–266PubMedCrossRef
Zurück zum Zitat Olah S, Füle M, Komlosi G, Varga C, Baldi R, Barzo P, Tamas G (2009) Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461:1278–1281PubMedPubMedCentralCrossRef Olah S, Füle M, Komlosi G, Varga C, Baldi R, Barzo P, Tamas G (2009) Regulation of cortical microcircuits by unitary GABA-mediated volume transmission. Nature 461:1278–1281PubMedPubMedCentralCrossRef
Zurück zum Zitat Omelchenko N, Bell R, Sesack SR (2009) Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur J Neurosci 30:1239–1250PubMedPubMedCentralCrossRef Omelchenko N, Bell R, Sesack SR (2009) Lateral habenula projections to dopamine and GABA neurons in the rat ventral tegmental area. Eur J Neurosci 30:1239–1250PubMedPubMedCentralCrossRef
Zurück zum Zitat Onaivi ES, Ishiguro H, Gong JP, Patel S, Perchuk A, Meozzi PA, Myers L, Mora Z, Tagliaferro P, Gardner E, Brusco A, Akinshola BE, Liu QR, Hope B, Iwasaki S, Arinami T, Teasenfitz L, Uhl GR (2006) Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann N Y Acad Sci 1074:514–536PubMedCrossRef Onaivi ES, Ishiguro H, Gong JP, Patel S, Perchuk A, Meozzi PA, Myers L, Mora Z, Tagliaferro P, Gardner E, Brusco A, Akinshola BE, Liu QR, Hope B, Iwasaki S, Arinami T, Teasenfitz L, Uhl GR (2006) Discovery of the presence and functional expression of cannabinoid CB2 receptors in brain. Ann N Y Acad Sci 1074:514–536PubMedCrossRef
Zurück zum Zitat Opland D, Sutton A, Woodworth H, Brown J, Bugescu R, Garcia A, Christensen L, Rhodes C, Myers M Jr, Leinninger G (2013) Loss of neurotensin receptor-1 disrupts the control of the mesolimbic dopamine system by leptin and promotes hedonic feeding and obesity. Mol Metab 2:423–434PubMedPubMedCentralCrossRef Opland D, Sutton A, Woodworth H, Brown J, Bugescu R, Garcia A, Christensen L, Rhodes C, Myers M Jr, Leinninger G (2013) Loss of neurotensin receptor-1 disrupts the control of the mesolimbic dopamine system by leptin and promotes hedonic feeding and obesity. Mol Metab 2:423–434PubMedPubMedCentralCrossRef
Zurück zum Zitat Parent A, Gravel S, Boucher R (1981) The origin of forebrain afferents to the habenula in rat, cat and monkey. Brain Res Bull 6:23–38PubMedCrossRef Parent A, Gravel S, Boucher R (1981) The origin of forebrain afferents to the habenula in rat, cat and monkey. Brain Res Bull 6:23–38PubMedCrossRef
Zurück zum Zitat Patel N, Itakura T, Gonzalez JM Jr, Schwartz SG, Fini ME (2013) GPR158, an orphan member of G protein-coupled receptor family C: glucocorticoid-stimulated expression and novel nuclear role. PLoS One 8:1–16CrossRef Patel N, Itakura T, Gonzalez JM Jr, Schwartz SG, Fini ME (2013) GPR158, an orphan member of G protein-coupled receptor family C: glucocorticoid-stimulated expression and novel nuclear role. PLoS One 8:1–16CrossRef
Zurück zum Zitat Petralia RS, Wang Y-X, Niedzielski AS, Wenthold RJ (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3 show unique postsynaptic, presynaptic, and glial localizations. Neuroscience 71:949–976PubMedCrossRef Petralia RS, Wang Y-X, Niedzielski AS, Wenthold RJ (1996) The metabotropic glutamate receptors, mGluR2 and mGluR3 show unique postsynaptic, presynaptic, and glial localizations. Neuroscience 71:949–976PubMedCrossRef
Zurück zum Zitat Poller WC, Madaia VI, Bernard R, Laube G, Veh RW (2013) A glutamatergic projection from the lateral hypothalamus targets VTA-projecting neurons in the lateral habenula of the rat. Brain Res 1507:45–60PubMedCrossRef Poller WC, Madaia VI, Bernard R, Laube G, Veh RW (2013) A glutamatergic projection from the lateral hypothalamus targets VTA-projecting neurons in the lateral habenula of the rat. Brain Res 1507:45–60PubMedCrossRef
Zurück zum Zitat Reichelt AC, Westbrook RF, Morris MJ (2015) Integration of reward signalling and appetite regulating peptide systems in the control of food-cue responses. Br J Pharmacol Epub ahead of print Reichelt AC, Westbrook RF, Morris MJ (2015) Integration of reward signalling and appetite regulating peptide systems in the control of food-cue responses. Br J Pharmacol Epub ahead of print
Zurück zum Zitat Ren J, Qin C, Hu F, Tan J, Qiu L, Zhao S, Feng G, Luo M (2011) Habenula ‘‘Cholinergic’’ neurons corelease glutamate and acetylcholine and activate postsynaptic neurons via distinct transmission modes. Neuron 69:445–452PubMedCrossRef Ren J, Qin C, Hu F, Tan J, Qiu L, Zhao S, Feng G, Luo M (2011) Habenula ‘‘Cholinergic’’ neurons corelease glutamate and acetylcholine and activate postsynaptic neurons via distinct transmission modes. Neuron 69:445–452PubMedCrossRef
Zurück zum Zitat Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:1–13CrossRef Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W, Smyth GK (2015) limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:1–13CrossRef
Zurück zum Zitat Rouse ST, Thomas TM, Levey AI (1997) Muscarinic acetylcholine receptor subtype, m2: diverse functional implications of differential synaptic localization. Life Sci 60:1031–1038PubMedCrossRef Rouse ST, Thomas TM, Levey AI (1997) Muscarinic acetylcholine receptor subtype, m2: diverse functional implications of differential synaptic localization. Life Sci 60:1031–1038PubMedCrossRef
Zurück zum Zitat Rouse ST, Edmunds SM, Yi H, Gilmor ML, Levey AI (2000) Localization of M2 muscarinic acetylcholine receptor protein in cholinergic and non-cholinergic terminals in rat hippocampus. Neurosci Lett 284:182–186PubMedCrossRef Rouse ST, Edmunds SM, Yi H, Gilmor ML, Levey AI (2000) Localization of M2 muscarinic acetylcholine receptor protein in cholinergic and non-cholinergic terminals in rat hippocampus. Neurosci Lett 284:182–186PubMedCrossRef
Zurück zum Zitat Rucinski M, Malendowicz LK (2009) Precerebellin-related genes and precerebellin 1 peptide in endocrine glands of the rat: pattern of their expression. Int J Mol Med 23:113–119PubMed Rucinski M, Malendowicz LK (2009) Precerebellin-related genes and precerebellin 1 peptide in endocrine glands of the rat: pattern of their expression. Int J Mol Med 23:113–119PubMed
Zurück zum Zitat Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1–27PubMed Schultz W (1998) Predictive reward signal of dopamine neurons. J Neurophysiol 80:1–27PubMed
Zurück zum Zitat Scott WR, Gelegen C, Chandarana K, Karra E, Yousseif A, Amouyal C, Choudhury AI, Andreelli F, Withers DJ, Batterham RL (2013) Differential Pre-mRNA splicing regulates Nnat isoforms in the hypothalamus after gastric bypass surgery in mice. PLoS One 8(3):e59407PubMedPubMedCentralCrossRef Scott WR, Gelegen C, Chandarana K, Karra E, Yousseif A, Amouyal C, Choudhury AI, Andreelli F, Withers DJ, Batterham RL (2013) Differential Pre-mRNA splicing regulates Nnat isoforms in the hypothalamus after gastric bypass surgery in mice. PLoS One 8(3):e59407PubMedPubMedCentralCrossRef
Zurück zum Zitat Segal JP, Stallings NR, Lee CE, Zhao L, Socci N, Viale A, Harris TM, Soares MB, Childs G, Elmquist JK, Parker KL, Friedman JM (2005) Use of laser-capture microdissection for the identification of marker genes for the ventromedial hypothalamic nucleus. J Neurosci 25:4181–4188PubMedCrossRef Segal JP, Stallings NR, Lee CE, Zhao L, Socci N, Viale A, Harris TM, Soares MB, Childs G, Elmquist JK, Parker KL, Friedman JM (2005) Use of laser-capture microdissection for the identification of marker genes for the ventromedial hypothalamic nucleus. J Neurosci 25:4181–4188PubMedCrossRef
Zurück zum Zitat Sego C, Goncalves L, Lima L, Furigo IC, Donato J Jr, Metzger M (2014) Lateral habenula and the rostromedial tegmental nucleus innervate neurochemically distinct subdivisions of the dorsal raphe nucleus in the rat. J Comp Neurol 522:1454–1484PubMedCrossRef Sego C, Goncalves L, Lima L, Furigo IC, Donato J Jr, Metzger M (2014) Lateral habenula and the rostromedial tegmental nucleus innervate neurochemically distinct subdivisions of the dorsal raphe nucleus in the rat. J Comp Neurol 522:1454–1484PubMedCrossRef
Zurück zum Zitat Shabel SJ, Proulx CD, Trias A, Murphy RT, Malinow R (2012) Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74:475–481PubMedPubMedCentralCrossRef Shabel SJ, Proulx CD, Trias A, Murphy RT, Malinow R (2012) Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74:475–481PubMedPubMedCentralCrossRef
Zurück zum Zitat Shelton L, Pendse G, Maleki N, Moulton EA, Lebel A, Becerra L, Borsook D (2012) Mapping pain activation and connectivity of the human habenula. J Neurophysiol 107:2633–2648PubMedPubMedCentralCrossRef Shelton L, Pendse G, Maleki N, Moulton EA, Lebel A, Becerra L, Borsook D (2012) Mapping pain activation and connectivity of the human habenula. J Neurophysiol 107:2633–2648PubMedPubMedCentralCrossRef
Zurück zum Zitat Shih P-Y, Engle SE, Oh G, Deshpande P, Puskar NL, Lester HA, Drenan RM (2014) Differential expression and function of nicotinic acetylcholine receptors in subdivisions of medial habenula. J Neurosci 34:9789–9802PubMedPubMedCentralCrossRef Shih P-Y, Engle SE, Oh G, Deshpande P, Puskar NL, Lester HA, Drenan RM (2014) Differential expression and function of nicotinic acetylcholine receptors in subdivisions of medial habenula. J Neurosci 34:9789–9802PubMedPubMedCentralCrossRef
Zurück zum Zitat Shughrue PJ, Lane MV, Merchenthaler I (1996) In situ hybridization analysis of the distribution of neurokinin-3 mRNA in the rat central nervous system. J Comp Neurol 372:395–414PubMedCrossRef Shughrue PJ, Lane MV, Merchenthaler I (1996) In situ hybridization analysis of the distribution of neurokinin-3 mRNA in the rat central nervous system. J Comp Neurol 372:395–414PubMedCrossRef
Zurück zum Zitat Simantov R, Kuhar MJ, Uhl GR, Snyder SH (1977) Opioid peptide enkephalin: immunohistochemical mapping in rat central nervous system. Proc Natl Acad Sci USA 74:2167–2171PubMedPubMedCentralCrossRef Simantov R, Kuhar MJ, Uhl GR, Snyder SH (1977) Opioid peptide enkephalin: immunohistochemical mapping in rat central nervous system. Proc Natl Acad Sci USA 74:2167–2171PubMedPubMedCentralCrossRef
Zurück zum Zitat Somogyi P, Takagi H (1982) A note on the use of picric acid-paraformaldehyde-glutaraldehyde fixative for correlated light and electron microscopic immunocytochemistry. Neuroscience 7:1779–1783PubMedCrossRef Somogyi P, Takagi H (1982) A note on the use of picric acid-paraformaldehyde-glutaraldehyde fixative for correlated light and electron microscopic immunocytochemistry. Neuroscience 7:1779–1783PubMedCrossRef
Zurück zum Zitat Sutton KA, Jungnickel MK, Wang Y, Cullen K, Lambert S, Florman HM (2004) Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Dev Biol 274:426–435PubMedCrossRef Sutton KA, Jungnickel MK, Wang Y, Cullen K, Lambert S, Florman HM (2004) Enkurin is a novel calmodulin and TRPC channel binding protein in sperm. Dev Biol 274:426–435PubMedCrossRef
Zurück zum Zitat Takeuchi F, Isono M, Katsuya T, Yamamoto K, Yokota M, Sugiyama T, Nabika T, Fujioka A, Ohnaka K, Asano H, Yamori Y, Yamaguchi S, Kobayashi S, Takayanagi R, Ogihara T, Kato N (2010) Blood pressure and hypertension are associated with 7 Loci in the Japanese population. Circulation 121:2302–2309PubMedCrossRef Takeuchi F, Isono M, Katsuya T, Yamamoto K, Yokota M, Sugiyama T, Nabika T, Fujioka A, Ohnaka K, Asano H, Yamori Y, Yamaguchi S, Kobayashi S, Takayanagi R, Ogihara T, Kato N (2010) Blood pressure and hypertension are associated with 7 Loci in the Japanese population. Circulation 121:2302–2309PubMedCrossRef
Zurück zum Zitat Tamaru Y, Nomura S, Mizuno N, Shigemoto R (2001) Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106:481–503PubMedCrossRef Tamaru Y, Nomura S, Mizuno N, Shigemoto R (2001) Distribution of metabotropic glutamate receptor mGluR3 in the mouse CNS: differential location relative to pre- and postsynaptic sites. Neuroscience 106:481–503PubMedCrossRef
Zurück zum Zitat Tamas G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902–1905PubMedCrossRef Tamas G, Lorincz A, Simon A, Szabadics J (2003) Identified sources and targets of slow inhibition in the neocortex. Science 299:1902–1905PubMedCrossRef
Zurück zum Zitat Tatemoto K, Lundberg JM, Jörnval H, Mutt V (1985) Neuropeptide K: isolation, structure, and biological acitivities of a novel brain tachykinin. Biochem Biophys Res Commun 128:947–953PubMedCrossRef Tatemoto K, Lundberg JM, Jörnval H, Mutt V (1985) Neuropeptide K: isolation, structure, and biological acitivities of a novel brain tachykinin. Biochem Biophys Res Commun 128:947–953PubMedCrossRef
Zurück zum Zitat Tortora GJ (2005) Principles of human anatomy. Wiley, New York Tortora GJ (2005) Principles of human anatomy. Wiley, New York
Zurück zum Zitat Ullsperger M, von Cramon DY (2003) Error monitoring using external feedback: specific roles of the habenular complex, the reward system, and the cingulate motor area revealed by functional magnetic resonance imaging. J Neurosci 23:4308–4314PubMed Ullsperger M, von Cramon DY (2003) Error monitoring using external feedback: specific roles of the habenular complex, the reward system, and the cingulate motor area revealed by functional magnetic resonance imaging. J Neurosci 23:4308–4314PubMed
Zurück zum Zitat Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555–582PubMedCrossRef Vertes RP, Fortin WJ, Crane AM (1999) Projections of the median raphe nucleus in the rat. J Comp Neurol 407:555–582PubMedCrossRef
Zurück zum Zitat Vrang N, Meyre D, Froguel P, Jelsing J, Tang-Christensen M, Vatin V, Mikkelsen JD, Thirstrup K, Larsen LK, Cullberg KB, Fahrenkrug J, Jacobson P, Sjöström L, Carlsson LM, Liu Y, Liu X, Deng HW, Larsen PJ (2010) The imprinted gene neuronatin is regulated by metabolic status and associated with obesity. Obesity 18:1289–1296PubMedCrossRef Vrang N, Meyre D, Froguel P, Jelsing J, Tang-Christensen M, Vatin V, Mikkelsen JD, Thirstrup K, Larsen LK, Cullberg KB, Fahrenkrug J, Jacobson P, Sjöström L, Carlsson LM, Liu Y, Liu X, Deng HW, Larsen PJ (2010) The imprinted gene neuronatin is regulated by metabolic status and associated with obesity. Obesity 18:1289–1296PubMedCrossRef
Zurück zum Zitat Wagner F, Stroh T, Veh RW (2014a) Correlating habenular subnuclei in rat and mouse by using topographic, morphological, and cytochemical criteria. J Comp Neurol 522:2650–2662PubMedCrossRef Wagner F, Stroh T, Veh RW (2014a) Correlating habenular subnuclei in rat and mouse by using topographic, morphological, and cytochemical criteria. J Comp Neurol 522:2650–2662PubMedCrossRef
Zurück zum Zitat Wagner F, French L, Veh RW (2014b) Transcriptomic-anatomic analysis of the mouse habenula uncovers a high molecular heterogeneity among neurons in the lateral complex, while gene expression in the medial complex largely obeys subnuclear boundaries. Brain Struct Funct Epub ahead of print Wagner F, French L, Veh RW (2014b) Transcriptomic-anatomic analysis of the mouse habenula uncovers a high molecular heterogeneity among neurons in the lateral complex, while gene expression in the medial complex largely obeys subnuclear boundaries. Brain Struct Funct Epub ahead of print
Zurück zum Zitat Wang S, Chen J-Z, Zhang Z, Huang Q, Gu S, Ying K, Xie Y, Mao Y (2002) Cloning, characterization, and expression of calcyphosine 2, a novel human gene encoding an EF-Hand Ca2-binding protein. Biochem Biophys Res Commun 291:414–420PubMedCrossRef Wang S, Chen J-Z, Zhang Z, Huang Q, Gu S, Ying K, Xie Y, Mao Y (2002) Cloning, characterization, and expression of calcyphosine 2, a novel human gene encoding an EF-Hand Ca2-binding protein. Biochem Biophys Res Commun 291:414–420PubMedCrossRef
Zurück zum Zitat Wang DG, Gong N, Luo B, Xu TL (2006) Absence of GABA type A signaling in adult medial habenular neurons. Neuroscience 141:133–141PubMedCrossRef Wang DG, Gong N, Luo B, Xu TL (2006) Absence of GABA type A signaling in adult medial habenular neurons. Neuroscience 141:133–141PubMedCrossRef
Zurück zum Zitat Wang C, Wang H, Zhang Y, Tang Z, Li K, Liu B (2014) Genome-wide analysis reveals artificial selection on coat colour and reproductive traits in Chinese domestic pigs. Mol Ecol Resour Epub ahead of print Wang C, Wang H, Zhang Y, Tang Z, Li K, Liu B (2014) Genome-wide analysis reveals artificial selection on coat colour and reproductive traits in Chinese domestic pigs. Mol Ecol Resour Epub ahead of print
Zurück zum Zitat Weiss T, Veh RW (2011) Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices. Neuroscience 172:74–93PubMedCrossRef Weiss T, Veh RW (2011) Morphological and electrophysiological characteristics of neurons within identified subnuclei of the lateral habenula in rat brain slices. Neuroscience 172:74–93PubMedCrossRef
Zurück zum Zitat Wickens AP (1987) Functional involvement of GABA agents in the habenular nuclei. Med Sci Res 15:35–36 Wickens AP (1987) Functional involvement of GABA agents in the habenular nuclei. Med Sci Res 15:35–36
Zurück zum Zitat Wisden W, Parker EM, Mahle CD, Grisel DA, Nowak HP, Yocca FD, Felder CC, Seeburg PH, Voigt MM (1993) Cloning and characterization of the rat 5HT(5B) receptor: evidence that the 5-HT(5B) receptor couples to a G-Protein in mammalian cell membranes. FEBS Lett 333:25–31PubMedCrossRef Wisden W, Parker EM, Mahle CD, Grisel DA, Nowak HP, Yocca FD, Felder CC, Seeburg PH, Voigt MM (1993) Cloning and characterization of the rat 5HT(5B) receptor: evidence that the 5-HT(5B) receptor couples to a G-Protein in mammalian cell membranes. FEBS Lett 333:25–31PubMedCrossRef
Zurück zum Zitat Zimmer DB, Chaplin J, Baldwin A, Rast M (2005) S100-mediated signal transduction in the nervous system and neurological diseases. Cell Mol Biol 5:201–214 Zimmer DB, Chaplin J, Baldwin A, Rast M (2005) S100-mediated signal transduction in the nervous system and neurological diseases. Cell Mol Biol 5:201–214
Zurück zum Zitat Zirlinger M, Anderson D (2003) Molecular dissection of the amygdala and its relevance to autism. Gene Brain Behav 2:282–294CrossRef Zirlinger M, Anderson D (2003) Molecular dissection of the amygdala and its relevance to autism. Gene Brain Behav 2:282–294CrossRef
Metadaten
Titel
Microarray analysis of transcripts with elevated expressions in the rat medial or lateral habenula suggest fast GABAergic excitation in the medial habenula and habenular involvement in the regulation of feeding and energy balance
verfasst von
Franziska Wagner
René Bernard
Christian Derst
Leon French
Rüdiger W. Veh
Publikationsdatum
18.02.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 9/2016
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1195-z

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