Top

Published in:

Open Access 01-01-2022 | Original Article

Stereological estimations and neurochemical characterization of neurons expressing GABAA and GABAB receptors in the rat pedunculopontine and laterodorsal tegmental nuclei

Authors: Esther Luquin, Beatriz Paternain, Inés Zugasti, Carmen Santomá, Elisa Mengual

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

Abstract

To better understand GABAergic transmission at two targets of basal ganglia downstream projections, the pedunculopontine (PPN) and laterodorsal (LDT) tegmental nuclei, the anatomical localization of GABAA and GABAB receptors was investigated in both nuclei. Specifically, the total number of neurons expressing the GABAA receptor γ2 subunit (GABAAR γ2) and the GABAB receptor R2 subunit (GABAB R2) in PPN and LDT was estimated using stereological methods, and the neurochemical phenotype of cells expressing each subunit was also determined. The mean number of non-cholinergic cells expressing GABAAR γ2 was 9850 ± 1856 in the PPN and 8285 ± 962 in the LDT, whereas those expressing GABAB R2 were 7310 ± 1970 and 9170 ± 1900 in the PPN and LDT, respectively. In addition, all cholinergic neurons in both nuclei co-expressed GABAAR γ2 and 95–98% of them co-expressed GABAB R2. Triple labeling using in situ hybridization revealed that 77% of GAD67 mRNA-positive cells in the PPT and 49% in the LDT expressed GABAAR γ2, while 90% (PPN) and 65% (LDT) of Vglut2 mRNA-positive cells also expressed GABAAR γ2. In contrast, a similar proportion (~2/3) of glutamatergic and GABAergic cells co-expressed GABAB R2 in both nuclei. The heterogeneous distribution of GABAAR and GABABR among non-cholinergic cells in PPN and LDT may give rise to physiological differences within each neurochemical subpopulation. In addition, the dissimilar proportion of GABAAR γ2-expressing glutamatergic and GABAergic neurons in the PPN and LDT may contribute to some of the functional differences found between the two nuclei.

Alakuijala A, Alakuijala J, Pasternack M (2006) Evidence for a functional role of GABA receptors in the rat mature hippocampus. Eur J Neurosci 23:514–520PubMed

Araujo F, Tan S, Ruano D, Schoemaker H, Benavides J et al (1996) Molecular and pharmacological characterization of native cortical gamma-aminobutyric acidA receptors containing both alpha1 and alpha3 subunits. J Biol Chem 271:27902–27911PubMed

Barberis A, Mozrzymas JW, Ortinski PI, Vicini S (2007) Desensitization and binding properties determine distinct alpha1beta2gamma2 and alpha3beta2gamma2 GABA(A) receptor-channel kinetic behavior. Eur J Neurosci 25:2726–2740PubMedPubMedCentral

Bartos M, Vida I, Frotscher M, Geiger JR, Jonas P (2001) Rapid signaling at inhibitory synapses in a dentate gyrus interneuron network. J Neurosci 21:2687–2698PubMedPubMedCentral

Benke D, Honer M, Michel C, Bettler B, Mohler H (1999) γ-Aminobutyric acid type B receptor splice variant proteins GBR1a and GBR1b are both associated with GBR2 in situ and display differential regional and subcellular distribution. J Biol Chem 274:27323–27330PubMed

Benke D, Fakitsas P, Roggenmoser C, Michel C, Rudolph U et al (2004) Analysis of the presence and abundance of GABAA receptors containing two different types of alpha subunits in murine brain using point-mutated alpha subunits. J Biol Chem 279:43654–43660PubMed

Bermejo PE, Jimenez CE, Torres CV, Avendano C (2003) Quantitative stereological evaluation of the gracile and cuneate nuclei and their projection neurons in the rat. J Comp Neurol 463:419–433PubMed

Bettler B, Tiao JY (2006) Molecular diversity, trafficking and subcellular localization of GABAB receptors. Pharmacol Ther 110:533–543PubMed

Bevan MD, Bolam JP (1995) Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J Neurosci 15:7105–7120PubMedPubMedCentral

Boccalaro IL, Cristia-Lara L, Schwerdel C, Fritschy JM, Rubi L (2019) Cell type-specific distribution of GABAA receptor subtypes in the mouse dorsal striatum. J Comp Neurol 527:2030–2046PubMed

Boucetta S, Cisse Y, Mainville L, Morales M, Jones BE (2014) Discharge profiles across the sleep-waking cycle of identified cholinergic, GABAergic, and glutamatergic neurons in the pontomesencephalic tegmentum of the rat. J Neurosci 34:4708–4727PubMedPubMedCentral

Bowery NG, Bettler B, Froestl W, Gallagher JW, Marshall F, Raiteri M, Bonner TI, Enna SJ (2002) International Union of Pharmacology. XXXIII. Mammalian gamma-aminobutyric acid(B) receptors: structure and function. Pharmacol Rev 54:247–264PubMed

Boyce RW, Dorph-Petersen KA, Lyck L, Gundersen HJ (2010) Design-based stereology: introduction to basic concepts and practical approaches for estimation of cell number. Toxicol Pathol 38:1011–1025PubMed

Boyes J, Bolam JP (2007) Localization of GABA receptors in the basal ganglia. Prog Brain Res 160:229–243PubMed

Broussard DM, Titley HK, Antflick J, Hampson DR (2011) Motor learning in the VOR: the cerebellar component. Exp Brain Res 210:451–463PubMed

Caggiano V, Leiras R, Goni-Erro H, Masini D, Bellardita C et al (2018) Midbrain circuits that set locomotor speed and gait selection. Nature 553:455–460PubMedPubMedCentral

Charles KJ, Evans ML, Robbins MJ, Calver AR, Leslie RA, Pangalos MN (2001) Comparative immunohistochemical localisation of GABA(B1a), GABA(B1b) and GABA(B2) subunits in rat brain, spinal cord and dorsal root ganglion. Neuroscience 106:447–467PubMed

Cornwall J, Cooper JD, Phillipson OT (1990) Afferent and efferent connections of the laterodorsal tegmental nucleus in the rat. Brain Res Bull 25:271–284PubMed

Datta S (2007) Activation of pedunculopontine tegmental PKA prevents GABAB receptor activation-mediated rapid eye movement sleep suppression in the freely moving rat. J Neurophysiol 97:3841–3850PubMed

Dautan D, Hacioglu Bay H, Bolam JP, Gerdjikov TV, Mena-Segovia J (2016a) Extrinsic sources of cholinergic innervation of the striatal complex: a whole-brain mapping analysis. Front Neuroanat 10:1PubMedPubMedCentral

Dautan D, Souza AS, Huerta-Ocampo I, Valencia M, Assous M et al (2016b) Segregated cholinergic transmission modulates dopamine neurons integrated in distinct functional circuits. Nat Neurosci 19:1025–1033PubMedPubMedCentral

Dorph-Petersen KA, Nyengaard JR, Gundersen HJ (2001) Tissue shrinkage and unbiased stereological estimation of particle number and size. J Microsc 204:232–246PubMed

Edley SM, Graybiel AM (1983) The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus, pars compacta. J Comp Neurol 217:187–215PubMed

Eliasen JN, Krall J, Frølund B, Kohlmeier KA (2020) Sex-specific alterations in GABA receptor-mediated responses in laterodorsal tegmentum are associated with prenatal exposure to nicotine. Dev Neurobiol 80:178–199PubMed

Erlander MG, Tillakaratne NJ, Feldblum S, Patel N, Tobin AJ (1991) Two genes encode distinct glutamate decarboxylases. Neuron 7:91–100PubMed

Essrich C, Lorez M, Benson JA, Fritschy JM, Luscher B (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nat Neurosci 1:563–571PubMed

Eyre MD, Renzi M, Farrant M, Nusser Z (2012) Setting the time course of inhibitory synaptic currents by mixing multiple GABA(A) receptor α subunit isoforms. J Neurosci 32:5853–5867PubMedPubMedCentral

Fogel SM, Smith CT, Beninger RJ (2010) Increased GABAergic activity in the region of the pedunculopontine and deep mesencephalic reticular nuclei reduces REM sleep and impairs learning in rats. Behav Neurosci 124:79–86PubMed

Frazao R, Nogueira MI, Wässle H (2007) Colocalization of synaptic GABAC-receptors with GABAA-receptors and glycine-receptors in the rodent central nervous system. Cell Tissue Res 330:1–15PubMed

Fritschy JM, Möhler H (1995) GABAA-receptor heterogeneity in the adult rat brain: differential regional and cellular distribution of seven major subunits. J Comp Neurol 359:154–194PubMed

Fritschy JM, Panzanelli P (2014) GABAA receptors and plasticity of inhibitory neurotransmission in the central nervous system. Eur J Neurosci 39:1845–1865PubMed

Fritschy JM, Benke D, Mertens S, Oertel WH, Bachi T et al (1992) Five subtypes of type A gamma-aminobutyric acid receptors identified in neurons by double and triple immunofluorescence staining with subunit-specific antibodies. Proc Natl Acad Sci USA 89:6726–6730PubMedPubMedCentral

Gao B, Hornung JP, Fritschy JM (1995) Identification of distinct GABAA-receptor subtypes in cholinergic and parvalbumin-positive neurons of the rat and marmoset medial septum-diagonal band complex. Neuroscience 65:101–117PubMed

Grofova I, Zhou M (1998) Nigral innervation of cholinergic and glutamatergic cells in the rat mesopontine tegmentum: light and electron microscopic anterograde tracing and immunohistochemical studies. J Comp Neurol 395:359–379PubMed

Gundersen HJ, Jensen EB (1987) The efficiency of systematic sampling in stereology and its prediction. J Microsc 147:229–263PubMed

Gundersen HJ, Jensen EB, Kieu K, Nielsen J (1999) The efficiency of systematic sampling in stereology–reconsidered. J Microsc 193:199–211PubMed

Gut NK, Winn P (2016) The pedunculopontine tegmental nucleus-A functional hypothesis from the comparative literature. Mov Disord 31:615–624PubMedPubMedCentral

Hallanger AE, Wainer BH (1988) Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J Comp Neurol 274:483–515PubMed

Hallanger AE, Levey AI, Lee HJ, Rye DB, Wainer BH (1987) The origins of cholinergic and other subcortical afferents to the thalamus in the rat. J Comp Neurol 262:105–124PubMed

Heinmiller A, Ting AKR, Vargas-Perez H, Yeh A, van der Kooy D (2009) Tegmental pedunculopontine glutamate and GABA-B synapses mediate morphine reward. Behav Neurosci 123:145–155PubMed

Henrich MT, Geibl FF, Lakshminarasimhan H, Stegmann A, Giasson BI, et al (2020) Determinants of seeding and spreading of alpha-synuclein pathology in the brain. Sci Adv 6.

Ikeda H, Akiyama G, Matsuzaki S, Sato M, Koshikawa N et al (2004) GABA_A receptors in the pedunculopontine tegmental nucleus play a crucial role in rat shell-specific dopamine-mediated, but not shell-specific acetylcholine-mediated, turning behaviour. Neuroscience 125:553–562PubMed

Kita T, Kita H (2011) Cholinergic and non-cholinergic mesopontine tegmental neurons projecting to the subthalamic nucleus in the rat. Eur J Neurosci 33:433–443PubMed

Kohlmeier KA, Kristiansen U (2010) GABAergic actions on cholinergic laterodorsal tegmental neurons: implications for control of behavioral state. Neuroscience 171:812–829PubMed

Kohlmeier KA, Vardar B, Christensen MH (2013) Gamma-Hydroxybutyric acid induces actions via the GABAB receptor in arousal and motor control-related nuclei: implications for therapeutic actions in behavioral state disorders. Neuroscience 248:261–277PubMed

Kroeger D, Ferrari LL, Petit G, Mahoney CE, Fuller PM et al (2017) Cholinergic, glutamatergic, and GABAergic neurons of the pedunculopontine tegmental nucleus have distinct effects on sleep/wake behavior in mice. J Neurosci 37:1352–1366PubMedPubMedCentral

Liang CL, Marks GA (2014) GABAA receptors are located in cholinergic terminals in the nucleus pontis oralis of the rat: implications for REM sleep control. Brain Res 1543:58–64PubMed

Lorincz A, Nusser Z (2008) Specificity of immunoreactions: the importance of testing specificity in each method. J Neurosci 28:9083–9086PubMedPubMedCentral

Luquin E, Pérez-Lorenzo E, Aymerich MS, Mengual E (2010) Two-color fluorescence labeling in acrolein-fixed brain tissue. J Histochem Cytochem 58:359–368PubMedPubMedCentral

Luquin E, Huerta I, Aymerich MS, Mengual E (2018) Stereological estimates of glutamatergic, GABAergic, and cholinergic neurons in the pedunculopontine and laterodorsal tegmental nuclei in the Rat. Front Neuroanat 12:34PubMedPubMedCentral

Luquin E, Paternain B, Mengual E (2017) Stereological estimations and neurochemical characterization of neurons expressing GABA_A receptor gamma 2 subunit in the rat pedunculopontine and laterodorsal tegmental nuclei. Program No. 592.09. 2017 Neuroscience Meeting Planner. Society for Neuroscience, Washington, DC

Maity B, Stewart A, Yang J, Loo L et al (2012) Regulator of G protein signaling 6 (RGS6) protein ensures coordination of motor movement by modulating GABAB receptor signaling. J Biol Chem 287:4972–4981PubMed

Margeta-Mitrovic M, Mitrovic I, Riley RC, Jan LY, Basbaum AI (1999) Immunohistochemical localization of GABA(B) receptors in the rat central nervous system. J Comp Neurol 405:299–321PubMed

McKernan RM, Whiting PJ (1996) Which GABAA-receptor subtypes really occur in the brain? Trends Neurosci 19:139–143PubMed

Mena-Segovia J (2016) Structural and functional considerations of the cholinergic brainstem. J Neural Transm (vienna) 123:731–736

Mena-Segovia J, Bolam JP, Magill PJ (2004) Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family? Trends Neurosci 27:585–588PubMed

Mena-Segovia J, Sims HM, Magill PJ, Bolam JP (2008) Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J Physiol 586:2947–2960PubMedPubMedCentral

Mena-Segovia J, Micklem BR, Nair-Roberts RG, Ungless MA, Bolam JP (2009) GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J Comp Neurol 515:397–408PubMed

Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185–1201PubMed

Micheva KD, Busse B, Weiler NC, O’Rourke N, Smith S (2010) Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. J Neuron 68(4):639–653

Milligan CJ, Buckley NJ, Garret M, Deuchars J, Deuchars SA (2004) Evidence for inhibition mediated by coassembly of GABAA and GABAC receptor subunits in native central neurons. J Neurosci 24:7241–7250PubMedPubMedCentral

Mitani A, Ito K, Hallanger AE, Wainer BH, Kataoka K et al (1988) Cholinergic projections from the laterodorsal and pedunculopontine tegmental nuclei to the pontine gigantocellular tegmental field in the cat. Brain Res 451:397–402PubMed

Mongia S, Luquin E, Mengual E (2015) Quantitative study of pallidotegmental projections contacting cholinergic, calbindin-, and calretinin- immunoreactive neurons in the rat pedunculopontine and laterodorsal tegmental nuclei. Program No. 340.01. 2015 Neuroscience Meeting Planner. Society for Neuroscience, Chicago, IL

Mongia S (2016) Quantitative analysis of synaptic contacts between the ventral pallidal and entopeduncular efferents and neurochemically diverse target neurons in the rat pedunculopontine and laterodorsal tegmental nuclei. Dissertation, University of Navarra, Spain

Mozrzymas JW, Barberis A, Vicini S (2007) GABAergic currents in RT and VB thalamic nuclei follow kinetic pattern of alpha3- and alpha1-subunit-containing GABAA receptors. Eur J Neurosci 26:657–665PubMedPubMedCentral

Nandi D, Aziz TZ, Giladi N, Winter J, Stein JF (2002) Reversal of akinesia in experimental parkinsonism by GABA antagonist microinjections in the pedunculopontine nucleus. Brain 125:2418–2430PubMed

Nassirpour R, Bahima L, Lalive AL, Lüscher C, Luján R, Slesinger PA (2010) Morphine- and CaMKII-dependent enhancement of GIRK channel signaling in hippocampal neurons. J Neurosci 30(40):13419–13430PubMedPubMedCentral

Nusser Z, Sieghart W, Somogyi P (1998) Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci 18:1693–1703PubMedPubMedCentral

Oakman SA, Faris PL, Kerr PE, Cozzari C, Hartman BK (1995) Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 15:5859–5869PubMedPubMedCentral

Olsen RW, Sieghart W (2009) GABA A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology 56:141–148PubMed

Pal D, Mallick BN (2004) GABA in pedunculo pontine tegmentum regulates spontaneous rapid eye movement sleep by acting on GABAA receptors in freely moving rats. Neurosci Lett 365:200–204PubMed

Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. Academic Press, New York

Pirker S, Schwarzer C, Wieselthaler A, Sieghart W, Sperk G (2000) GABA(A) receptors: immunocytochemical distribution of 13 subunits in the adult rat brain. Neuroscience 101:815–850PubMed

Rodríguez-Pallares J, Labandeira-Garcia JL, Munoz A, Caruncho HJ (2000) Morphology and neurochemistry of two striatal neuronal subtypes expressing the GABA(A) receptor alpha3-subunit in the rat. Brain Res 876:124–130PubMed

Rodríguez-Pallares J, Caruncho HJ, López-Real A, Wójcik S, Guerra MJ et al (2001) Rat brain cholinergic, dopaminergic, noradrenergic and serotonergic neurons express GABAA receptors derived from the alpha3 subunit. Receptors Channels 7:471–478PubMed

Ros H, Magill PJ, Moss J, Bolam JP, Mena-Segovia J (2010) Distinct types of non-cholinergic pedunculopontine neurons are differentially modulated during global brain states. Neuroscience 170:78–91PubMed

Roseberry TK, Lee AM, Lalive AL, Wilbrecht L, Bonci A et al (2016) Cell-type-specific control of brainstem locomotor circuits by basal ganglia. Cell 164:526–537PubMedPubMedCentral

Rye DB, Saper CB, Lee HJ, Wainer BH (1987) Pedunculopontine tegmental nucleus of the rat: cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J Comp Neurol 259:483–528PubMed

Saitoh K, Hattori S, Song WJ, Isa T, Takakusaki K (2003) Nigral GABAergic inhibition upon cholinergic neurons in the rat pedunculopontine tegmental nucleus. Eur J Neurosci 18:879–886PubMed

Sakai K (2012) Discharge properties of presumed cholinergic and noncholinergic laterodorsal tegmental neurons related to cortical activation in non-anesthetized mice. Neuroscience 224:172–190PubMed

Sapin E, Lapray D, Berod A, Goutagny R, Leger L et al (2009) Localization of the brainstem GABAergic neurons controlling paradoxical (REM) sleep. PLoS ONE 4:e4272PubMedPubMedCentral

Semba K, Fibiger HC (1992) Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and anterograde transport and immunohistochemical study. J Comp Neurol 323:387–410PubMed

Semba K, Reiner PB, Fibiger HC (1990) Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 38:643–654PubMed

Sergeeva OA, Eriksson KS, Sharonova I, Vorobjev V, Haas H (2002) GABA(A) receptor heterogeneity in histaminergic neurons. Eur J Neurosci 16:1472–1482PubMed

Shen W, Nan C, Nelson PT, Ripps H, Slaughter MM (2017) GABAB receptor attenuation of GABAA currents in neurons of the mammalian central nervous system. Physiol Rep 5:e13129. https://doi.org/10.14814/phy2.13129CrossRefPubMedPubMedCentral

Sherman D, Fuller PM, Marcus J, Yu J, Zhang P et al (2015) Anatomical location of the mesencephalic locomotor region and its possible role in locomotion, posture, cataplexy, and parkinsonism. Front Neurol 6:140PubMedPubMedCentral

Shink E, Sidibé M, Smith Y (1997) Efferent connections of the internal globus pallidus in the squirrel monkey: II. Topography and synaptic organization of pallidal efferents to the pedunculopontine nucleus. J Comp Neurol 382:348–363PubMed

Shiromani PJ, Armstrong DM, Gillin JC (1988) Cholinergic neurons from the dorsolateral pons project to the medial pons: a WGA-HRP and choline acetyltransferase immunohistochemical study. Neurosci Lett 95:19–23PubMed

Steininger TL, Rye DB, Wainer BH (1992) Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat. I. Retrograde tracing studies. J Comp Neurol 321:515–543PubMed

Stornetta RL, Sevigny CP, Guyenet PG (2002a) Vesicular glutamate transporter DNPI/VGLUT2 mRNA is present in C1 and several other groups of brainstem catecholaminergic neurons. J Comp Neurol 444(3):191–206PubMed

Stornetta RL, Sevigny CP, Schreihofer AM, Rosin DL, Guyenet PG (2002b) Vesicular glutamate transporter DNPI/VGLUT2 is expressed by both C1 adrenergic and nonaminergic presympathetic vasomotor neurons of the rat medulla. J Comp Neurol 444(3):207–220PubMed

Takakusaki K, Shiroyama T, Kitai ST (1997) Two types of cholinergic neurons in the rat tegmental pedunculopontine nucleus: electrophysiological and morphological characterization. Neuroscience 79:1089–1109PubMed

Takakusaki K, Chiba R, Nozu T, Okumura T (2016) Brainstem control of locomotion and muscle tone with special reference to the role of the mesopontine tegmentum and medullary reticulospinal systems. J Neural Transm (vienna) 123:695–729

Tia S, Wang JF, Kotchabhakdi N, Vicini S (1996) Distinct deactivation and desensitization kinetics of recombinant GABAA receptors. Neuropharmacology 35:1375–1382PubMed

Tillakaratne NJ, Erlander MG, Collard MW, Greif KF, Tobin AJ (1992) Glutamate decarboxylases in nonneural cells of rat testis and oviduct: differential expression of GAD65 and GAD67. J Neurochem 58(2):618–627PubMed

Torterolo P, Morales FR, Chase MH (2002) GABAergic mechanisms in the pedunculopontine tegmental nucleus of the cat promote active (REM) sleep. Brain Res 944:1–9PubMed

Ulloor J, Mavanji V, Saha S, Siwek DF, Datta S (2004) Spontaneous REM sleep is modulated by the activation of the pedunculopontine tegmental GABAB receptors in the freely moving rat. J Neurophysiol 91:1822–1831PubMed

Vassias I, Lecolle S, Vidal PP, de Waele C (2005) Modulation of GABA receptor subunits in rat facial motoneurons after axotomy. Brain Res Mol Brain Res 135:260–275PubMed

Vincent SR, Satoh K, Armstrong DM, Fibiger HC (1983) NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci Lett 43:31–36PubMed

Wang HL, Morales M (2009) Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur J Neurosci 29:340–358PubMed

Weber F, Hoang Do JP, Chung S, Beier KT, Bikov M et al (2018) Regulation of REM and non-REM sleep by periaqueductal GABAergic neurons. Nat Commun 9:354PubMedPubMedCentral

Wei W, Zhang N, Peng Z, Houser CR, Mody I (2003) Perisynaptic localization of delta subunit-containing GABA(A) receptors and their activation by GABA spillover in the mouse dentate gyrus. J Neurosci 23:10650–10661PubMedPubMedCentral

West MJ, Gundersen HJ (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296:1–22PubMed

Woolf NJ, Butcher LL (1986) Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 16:603–637PubMed

Xiao C, Cho JR, Zhou C, Treweek JB, Chan K et al (2016) Cholinergic mesopontine signals govern locomotion and reward through dissociable midbrain pathways. Neuron 90:333–347PubMedPubMedCentral

Yang H, Yang J, Xi W, Hao S, Luo B et al (2016) Laterodorsal tegmentum interneuron subtypes oppositely regulate olfactory cue-induced innate fear. Nat Neurosci 19:283–289PubMed

Ye M, Garcia-Rill E (2009) Potentiating effect of eszopiclone on GABA(A) receptor-mediated responses in pedunculopontine neurons. Sleep 32:879–887PubMedPubMedCentral

Ye Z, Yu X, Houston CM, Aboukhalil Z, Franks NP et al (2017) Fast and slow inhibition in the visual thalamus is influenced by allocating GABAA receptors with different gamma subunits. Front Cell Neurosci 11:95PubMedPubMedCentral

Title: Stereological estimations and neurochemical characterization of neurons expressing GABAA and GABAB receptors in the rat pedunculopontine and laterodorsal tegmental nuclei
Authors: Esther Luquin
Beatriz Paternain
Inés Zugasti
Carmen Santomá
Elisa Mengual
Publication date: 01-01-2022
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 1/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-021-02375-9

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Stereological estimations and neurochemical characterization of neurons expressing GABAA and GABAB receptors in the rat pedunculopontine and laterodorsal tegmental nuclei

Abstract

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 1/2022

Different changes in pre- and postsynaptic components in the hippocampal CA1 subfield after transient global cerebral ischemia

Structure can predict function in the human brain: a graph neural network deep learning model of functional connectivity and centrality based on structural connectivity

Application of the anatomical fiducials framework to a clinical dataset of patients with Parkinson’s disease

Magnetic resonance fingerprinting residual signals can disassociate human grey matter regions

Topographical functional correlates of interindividual differences in executive functions in young healthy twins

Correction to: Wrist and finger motor representations embedded in the cerebral and cerebellar resting-state activation