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Published in: Brain Structure and Function 4/2017

Open Access 01-05-2017 | Original Article

Anatomical and molecular characterization of dopamine D1 receptor-expressing neurons of the mouse CA1 dorsal hippocampus

Authors: Emma Puighermanal, Laura Cutando, Jihane Boubaker-Vitre, Eve Honoré, Sophie Longueville, Denis Hervé, Emmanuel Valjent

Published in: Brain Structure and Function | Issue 4/2017

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Abstract

In the hippocampus, a functional role of dopamine D1 receptors (D1R) in synaptic plasticity and memory processes has been suggested by electrophysiological and pharmacological studies. However, comprehension of their function remains elusive due to the lack of knowledge on the precise localization of D1R expression among the diversity of interneuron populations. Using BAC transgenic mice expressing enhanced green fluorescent protein under the control of D1R promoter, we examined the molecular identity of D1R-containing neurons within the CA1 subfield of the dorsal hippocampus. In agreement with previous findings, our analysis revealed that these neurons are essentially GABAergic interneurons, which express several neurochemical markers, including calcium-binding proteins, neuropeptides, and receptors among others. Finally, by using different tools comprising cell type-specific isolation of mRNAs bound to tagged-ribosomes, we provide solid data indicating that D1R is present in a large proportion of interneurons expressing dopamine D2 receptors. Altogether, our study indicates that D1Rs are expressed by different classes of interneurons in all layers examined and not by pyramidal cells, suggesting that CA1 D1R mostly acts via modulation of GABAergic interneurons.
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Literature
go back to reference Armstrong C, Krook-Magnuson E, Soltesz I (2012) Neurogliaform and ivy cells: a major family of nNOS expressing GABAergic neurons. Front Neural Circuits 6:23CrossRefPubMedPubMedCentral Armstrong C, Krook-Magnuson E, Soltesz I (2012) Neurogliaform and ivy cells: a major family of nNOS expressing GABAergic neurons. Front Neural Circuits 6:23CrossRefPubMedPubMedCentral
go back to reference Bertran-Gonzalez J, Bosch C, Maroteaux M, Matamales M, Herve D, Valjent E, Girault JA (2008) Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 28(22):5671–5685CrossRefPubMed Bertran-Gonzalez J, Bosch C, Maroteaux M, Matamales M, Herve D, Valjent E, Girault JA (2008) Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J Neurosci 28(22):5671–5685CrossRefPubMed
go back to reference Bertran-Gonzalez J, Hervé D, Girault JA, Valjent E (2010) What is the degree of segregation between striatonigral and striatopallidal projections? Front Neuroanat 4. doi:10.3389/fnana.2010.00136 Bertran-Gonzalez J, Hervé D, Girault JA, Valjent E (2010) What is the degree of segregation between striatonigral and striatopallidal projections? Front Neuroanat 4. doi:10.​3389/​fnana.​2010.​00136
go back to reference Bethus I, Tse D, Morris RG (2010) Dopamine and memory: modulation of the persistence of memory for novel hippocampal NMDA receptor-dependent paired associates. J Neurosci 30(5):1610–1618CrossRefPubMed Bethus I, Tse D, Morris RG (2010) Dopamine and memory: modulation of the persistence of memory for novel hippocampal NMDA receptor-dependent paired associates. J Neurosci 30(5):1610–1618CrossRefPubMed
go back to reference Boyson SJ, McGonigle P, Molinoff PB (1986) Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain. J Neurosci 6(11):3177–3188PubMed Boyson SJ, McGonigle P, Molinoff PB (1986) Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain. J Neurosci 6(11):3177–3188PubMed
go back to reference Broussard JI, Yang K, Levine AT, Tsetsenis T, Jenson D, Cao F, Garcia I, Arenkiel BR, Zhou FM, De Biasi M et al (2016) Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the hippocampus. Cell Rep 14(8):1930–1939CrossRefPubMedPubMedCentral Broussard JI, Yang K, Levine AT, Tsetsenis T, Jenson D, Cao F, Garcia I, Arenkiel BR, Zhou FM, De Biasi M et al (2016) Dopamine regulates aversive contextual learning and associated in vivo synaptic plasticity in the hippocampus. Cell Rep 14(8):1930–1939CrossRefPubMedPubMedCentral
go back to reference Chittajallu R, Craig MT, McFarland A, Yuan X, Gerfen S, Tricoire L, Erkkila B, Barron SC, Lopez CM, Liang BJ et al (2013) Dual origins of functionally distinct O-LM interneurons revealed by differential 5-HT(3A)R expression. Nat Neurosci 16(11):1598–1607CrossRefPubMedPubMedCentral Chittajallu R, Craig MT, McFarland A, Yuan X, Gerfen S, Tricoire L, Erkkila B, Barron SC, Lopez CM, Liang BJ et al (2013) Dual origins of functionally distinct O-LM interneurons revealed by differential 5-HT(3A)R expression. Nat Neurosci 16(11):1598–1607CrossRefPubMedPubMedCentral
go back to reference Franklin K, Paxinos G (2007) The mouse brain in stereotaxic coordinates, 3rd edn. Elsevier, Amsterdam Franklin K, Paxinos G (2007) The mouse brain in stereotaxic coordinates, 3rd edn. Elsevier, Amsterdam
go back to reference Fremeau RT Jr, Duncan GE, Fornaretto MG, Dearry A, Gingrich JA, Breese GR, Caron MG (1991) Localization of D1 dopamine receptor mRNA in brain supports a role in cognitive, affective, and neuroendocrine aspects of dopaminergic neurotransmission. Proc Natl Acad Sci USA 88(9):3772–3776CrossRefPubMedPubMedCentral Fremeau RT Jr, Duncan GE, Fornaretto MG, Dearry A, Gingrich JA, Breese GR, Caron MG (1991) Localization of D1 dopamine receptor mRNA in brain supports a role in cognitive, affective, and neuroendocrine aspects of dopaminergic neurotransmission. Proc Natl Acad Sci USA 88(9):3772–3776CrossRefPubMedPubMedCentral
go back to reference Fuentealba P, Begum R, Capogna M, Jinno S, Marton LF, Csicsvari J, Thomson A, Somogyi P, Klausberger T (2008) Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 57(6):917–929CrossRefPubMedPubMedCentral Fuentealba P, Begum R, Capogna M, Jinno S, Marton LF, Csicsvari J, Thomson A, Somogyi P, Klausberger T (2008) Ivy cells: a population of nitric-oxide-producing, slow-spiking GABAergic neurons and their involvement in hippocampal network activity. Neuron 57(6):917–929CrossRefPubMedPubMedCentral
go back to reference Furini CR, Myskiw JC, Schmidt BE, Marcondes LA, Izquierdo I (2014) D1 and D5 dopamine receptors participate on the consolidation of two different memories. Behav Brain Res 271:212–217CrossRefPubMed Furini CR, Myskiw JC, Schmidt BE, Marcondes LA, Izquierdo I (2014) D1 and D5 dopamine receptors participate on the consolidation of two different memories. Behav Brain Res 271:212–217CrossRefPubMed
go back to reference Gangarossa G, Longueville S, De Bundel D, Perroy J, Herve D, Girault JA, Valjent E (2012) Characterization of dopamine D1 and D2 receptor-expressing neurons in the mouse hippocampus. Hippocampus 22(12):2199–2207CrossRefPubMed Gangarossa G, Longueville S, De Bundel D, Perroy J, Herve D, Girault JA, Valjent E (2012) Characterization of dopamine D1 and D2 receptor-expressing neurons in the mouse hippocampus. Hippocampus 22(12):2199–2207CrossRefPubMed
go back to reference Gasbarri A, Packard MG, Campana E, Pacitti C (1994a) Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33(4):445–452CrossRefPubMed Gasbarri A, Packard MG, Campana E, Pacitti C (1994a) Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat. Brain Res Bull 33(4):445–452CrossRefPubMed
go back to reference Gasbarri A, Verney C, Innocenzi R, Campana E, Pacitti C (1994b) Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study. Brain Res 668(1–2):71–79CrossRefPubMed Gasbarri A, Verney C, Innocenzi R, Campana E, Pacitti C (1994b) Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study. Brain Res 668(1–2):71–79CrossRefPubMed
go back to reference Gasbarri A, Sulli A, Packard MG (1997) The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21(1):1–22CrossRefPubMed Gasbarri A, Sulli A, Packard MG (1997) The dopaminergic mesencephalic projections to the hippocampal formation in the rat. Prog Neuropsychopharmacol Biol Psychiatry 21(1):1–22CrossRefPubMed
go back to reference Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME et al (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425(6961):917–925CrossRefPubMed Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME et al (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425(6961):917–925CrossRefPubMed
go back to reference Heath FC, Jurkus R, Bast T, Pezze MA, Lee JL, Voigt JP, Stevenson CW (2015) Dopamine D1-like receptor signalling in the hippocampus and amygdala modulates the acquisition of contextual fear conditioning. Psychopharmacology 232(14):2619–2629CrossRefPubMedPubMedCentral Heath FC, Jurkus R, Bast T, Pezze MA, Lee JL, Voigt JP, Stevenson CW (2015) Dopamine D1-like receptor signalling in the hippocampus and amygdala modulates the acquisition of contextual fear conditioning. Psychopharmacology 232(14):2619–2629CrossRefPubMedPubMedCentral
go back to reference Horvitz JC, Stewart T, Jacobs BL (1997) Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat. Brain Res 759(2):251–258CrossRefPubMed Horvitz JC, Stewart T, Jacobs BL (1997) Burst activity of ventral tegmental dopamine neurons is elicited by sensory stimuli in the awake cat. Brain Res 759(2):251–258CrossRefPubMed
go back to reference Huang Q, Zhou D, Chase K, Gusella JF, Aronin N, DiFiglia M (1992) Immunohistochemical localization of the D1 dopamine receptor in rat brain reveals its axonal transport, pre- and postsynaptic localization, and prevalence in the basal ganglia, limbic system, and thalamic reticular nucleus. Proc Natl Acad Sci USA 89(24):11988–11992CrossRefPubMedPubMedCentral Huang Q, Zhou D, Chase K, Gusella JF, Aronin N, DiFiglia M (1992) Immunohistochemical localization of the D1 dopamine receptor in rat brain reveals its axonal transport, pre- and postsynaptic localization, and prevalence in the basal ganglia, limbic system, and thalamic reticular nucleus. Proc Natl Acad Sci USA 89(24):11988–11992CrossRefPubMedPubMedCentral
go back to reference Jinno S, Kosaka T (2002) Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J Comp Neurol 449(1):1–25CrossRefPubMed Jinno S, Kosaka T (2002) Patterns of expression of calcium binding proteins and neuronal nitric oxide synthase in different populations of hippocampal GABAergic neurons in mice. J Comp Neurol 449(1):1–25CrossRefPubMed
go back to reference Karunakaran S, Chowdhury A, Donato F, Quairiaux C, Michel CM, Caroni P (2016) PV plasticity sustained through D1/5 dopamine signaling required for long-term memory consolidation. Nat Neurosci 19(3):454–464CrossRefPubMed Karunakaran S, Chowdhury A, Donato F, Quairiaux C, Michel CM, Caroni P (2016) PV plasticity sustained through D1/5 dopamine signaling required for long-term memory consolidation. Nat Neurosci 19(3):454–464CrossRefPubMed
go back to reference Kern A, Mavrikaki M, Ullrich C, Albarran-Zeckler R, Brantley AF, Smith RG (2015) Hippocampal dopamine/DRD1 signaling dependent on the Ghrelin receptor. Cell 163(5):1176–1190CrossRefPubMedPubMedCentral Kern A, Mavrikaki M, Ullrich C, Albarran-Zeckler R, Brantley AF, Smith RG (2015) Hippocampal dopamine/DRD1 signaling dependent on the Ghrelin receptor. Cell 163(5):1176–1190CrossRefPubMedPubMedCentral
go back to reference Klausberger T (2009) GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur J Neurosci 30(6):947–957CrossRefPubMed Klausberger T (2009) GABAergic interneurons targeting dendrites of pyramidal cells in the CA1 area of the hippocampus. Eur J Neurosci 30(6):947–957CrossRefPubMed
go back to reference Kwon OB, Paredes D, Gonzalez CM, Neddens J, Hernandez L, Vullhorst D, Buonanno A (2008) Neuregulin-1 regulates LTP at CA1 hippocampal synapses through activation of dopamine D4 receptors. Proc Natl Acad Sci USA 105(40):15587–15592CrossRefPubMedPubMedCentral Kwon OB, Paredes D, Gonzalez CM, Neddens J, Hernandez L, Vullhorst D, Buonanno A (2008) Neuregulin-1 regulates LTP at CA1 hippocampal synapses through activation of dopamine D4 receptors. Proc Natl Acad Sci USA 105(40):15587–15592CrossRefPubMedPubMedCentral
go back to reference Ladepeche L, Dupuis JP, Bouchet D, Doudnikoff E, Yang L, Campagne Y, Bezard E, Hosy E, Groc L (2013a) Single-molecule imaging of the functional crosstalk between surface NMDA and dopamine D1 receptors. Proc Natl Acad Sci USA 110(44):18005–18010CrossRefPubMedPubMedCentral Ladepeche L, Dupuis JP, Bouchet D, Doudnikoff E, Yang L, Campagne Y, Bezard E, Hosy E, Groc L (2013a) Single-molecule imaging of the functional crosstalk between surface NMDA and dopamine D1 receptors. Proc Natl Acad Sci USA 110(44):18005–18010CrossRefPubMedPubMedCentral
go back to reference Ladepeche L, Yang L, Bouchet D, Groc L (2013b) Regulation of dopamine D1 receptor dynamics within the postsynaptic density of hippocampal glutamate synapses. PLoS One 8(9):e74512CrossRefPubMedPubMedCentral Ladepeche L, Yang L, Bouchet D, Groc L (2013b) Regulation of dopamine D1 receptor dynamics within the postsynaptic density of hippocampal glutamate synapses. PLoS One 8(9):e74512CrossRefPubMedPubMedCentral
go back to reference Lammel S, Lim BK, Ran C, Huang KW, Betley MJ, Tye KM, Deisseroth K, Malenka RC (2012) Input-specific control of reward and aversion in the ventral tegmental area. Nature 491(7423):212–217CrossRefPubMedPubMedCentral Lammel S, Lim BK, Ran C, Huang KW, Betley MJ, Tye KM, Deisseroth K, Malenka RC (2012) Input-specific control of reward and aversion in the ventral tegmental area. Nature 491(7423):212–217CrossRefPubMedPubMedCentral
go back to reference Lemon N, Manahan-Vaughan D (2006) Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci 26(29):7723–7729CrossRefPubMed Lemon N, Manahan-Vaughan D (2006) Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long-term potentiation and long-term depression. J Neurosci 26(29):7723–7729CrossRefPubMed
go back to reference Lisman JE, Grace AA (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46(5):703–713CrossRefPubMed Lisman JE, Grace AA (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46(5):703–713CrossRefPubMed
go back to reference Ljungberg T, Apicella P, Schultz W (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67(1):145–163PubMed Ljungberg T, Apicella P, Schultz W (1992) Responses of monkey dopamine neurons during learning of behavioral reactions. J Neurophysiol 67(1):145–163PubMed
go back to reference Mansour A, Meador-Woodruff JH, Bunzow JR, Civelli O, Akil H, Watson SJ (1990) Localization of dopamine D2 receptor mRNA and D1 and D2 receptor binding in the rat brain and pituitary: an in situ hybridization-receptor autoradiographic analysis. J Neurosci 10(8):2587–2600PubMed Mansour A, Meador-Woodruff JH, Bunzow JR, Civelli O, Akil H, Watson SJ (1990) Localization of dopamine D2 receptor mRNA and D1 and D2 receptor binding in the rat brain and pituitary: an in situ hybridization-receptor autoradiographic analysis. J Neurosci 10(8):2587–2600PubMed
go back to reference Mansour A, Meador-Woodruff JH, Zhou QY, Civelli O, Akil H, Watson SJ (1991) A comparison of D1 receptor binding and mRNA in rat brain using receptor autoradiographic and in situ hybridization techniques. Neuroscience 45(2):359–371CrossRefPubMed Mansour A, Meador-Woodruff JH, Zhou QY, Civelli O, Akil H, Watson SJ (1991) A comparison of D1 receptor binding and mRNA in rat brain using receptor autoradiographic and in situ hybridization techniques. Neuroscience 45(2):359–371CrossRefPubMed
go back to reference Marchionni I, Takacs VT, Nunzi MG, Mugnaini E, Miller RJ, Maccaferri G (2010) Distinctive properties of CXC chemokine receptor 4-expressing Cajal–Retzius cells versus GABAergic interneurons of the postnatal hippocampus. J Physiol 588(Pt 15):2859–2878CrossRefPubMedPubMedCentral Marchionni I, Takacs VT, Nunzi MG, Mugnaini E, Miller RJ, Maccaferri G (2010) Distinctive properties of CXC chemokine receptor 4-expressing Cajal–Retzius cells versus GABAergic interneurons of the postnatal hippocampus. J Physiol 588(Pt 15):2859–2878CrossRefPubMedPubMedCentral
go back to reference Matyas F, Freund TF, Gulyas AI (2004) Immunocytochemically defined interneuron populations in the hippocampus of mouse strains used in transgenic technology. Hippocampus 14(4):460–481CrossRefPubMed Matyas F, Freund TF, Gulyas AI (2004) Immunocytochemically defined interneuron populations in the hippocampus of mouse strains used in transgenic technology. Hippocampus 14(4):460–481CrossRefPubMed
go back to reference McNamara CG, Tejero-Cantero A, Trouche S, Campo-Urriza N, Dupret D (2014) Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat Neurosci 17(12):1658–1660CrossRefPubMedPubMedCentral McNamara CG, Tejero-Cantero A, Trouche S, Campo-Urriza N, Dupret D (2014) Dopaminergic neurons promote hippocampal reactivation and spatial memory persistence. Nat Neurosci 17(12):1658–1660CrossRefPubMedPubMedCentral
go back to reference Otmakhova NA, Lisman JE (1999) Dopamine selectively inhibits the direct cortical pathway to the CA1 hippocampal region. J Neurosci 19(4):1437–1445PubMed Otmakhova NA, Lisman JE (1999) Dopamine selectively inhibits the direct cortical pathway to the CA1 hippocampal region. J Neurosci 19(4):1437–1445PubMed
go back to reference Pawelzik H, Hughes DI, Thomson AM (2002) Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol 443(4):346–367CrossRefPubMed Pawelzik H, Hughes DI, Thomson AM (2002) Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneurones in CA1 of the adult rat hippocampus. J Comp Neurol 443(4):346–367CrossRefPubMed
go back to reference Poulin JF, Zou J, Drouin-Ouellet J, Kim KY, Cicchetti F, Awatramani RB (2014) Defining midbrain dopaminergic neuron diversity by single-cell gene expression profiling. Cell Rep 9(3):930–943CrossRefPubMedPubMedCentral Poulin JF, Zou J, Drouin-Ouellet J, Kim KY, Cicchetti F, Awatramani RB (2014) Defining midbrain dopaminergic neuron diversity by single-cell gene expression profiling. Cell Rep 9(3):930–943CrossRefPubMedPubMedCentral
go back to reference Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M (2005) Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25(29):6775–6786CrossRefPubMed Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M (2005) Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 25(29):6775–6786CrossRefPubMed
go back to reference Puighermanal E, Biever A, Espallergues J, Gangarossa G, De Bundel D, Valjent E (2015) drd2-cre:ribotag mouse line unravels the possible diversity of dopamine d2 receptor-expressing cells of the dorsal mouse hippocampus. Hippocampus 25(7):858–875CrossRefPubMed Puighermanal E, Biever A, Espallergues J, Gangarossa G, De Bundel D, Valjent E (2015) drd2-cre:ribotag mouse line unravels the possible diversity of dopamine d2 receptor-expressing cells of the dorsal mouse hippocampus. Hippocampus 25(7):858–875CrossRefPubMed
go back to reference Rocchetti J, Isingrini E, Dal Bo G, Sagheby S, Menegaux A, Tronche F, Levesque D, Moquin L, Gratton A, Wong TP, Rubinstein M, Giros B (2015) Presynaptic D2 dopamine receptors control long-term depression expression and memory processes in the temporal hippocampus. Biol Psychiatry 77(6):513–525 Rocchetti J, Isingrini E, Dal Bo G, Sagheby S, Menegaux A, Tronche F, Levesque D, Moquin L, Gratton A, Wong TP, Rubinstein M, Giros B (2015) Presynaptic D2 dopamine receptors control long-term depression expression and memory processes in the temporal hippocampus. Biol Psychiatry 77(6):513–525
go back to reference Rosen ZB, Cheung S, Siegelbaum SA (2015) Midbrain dopamine neurons bidirectionally regulate CA3-CA1 synaptic drive. Nat Neurosci 18(12):1763–1771CrossRefPubMed Rosen ZB, Cheung S, Siegelbaum SA (2015) Midbrain dopamine neurons bidirectionally regulate CA3-CA1 synaptic drive. Nat Neurosci 18(12):1763–1771CrossRefPubMed
go back to reference Rossato JI, Bevilaqua LR, Izquierdo I, Medina JH, Cammarota M (2009) Dopamine controls persistence of long-term memory storage. Science 325(5943):1017–1020CrossRefPubMed Rossato JI, Bevilaqua LR, Izquierdo I, Medina JH, Cammarota M (2009) Dopamine controls persistence of long-term memory storage. Science 325(5943):1017–1020CrossRefPubMed
go back to reference Sanz E, Yang L, Su T, Morris DR, McKnight GS, Amieux PS (2009) Cell-type-specific isolation of ribosome-associated mRNA from complex tissues. Proc Natl Acad Sci USA 106(33):13939–13944CrossRefPubMedPubMedCentral Sanz E, Yang L, Su T, Morris DR, McKnight GS, Amieux PS (2009) Cell-type-specific isolation of ribosome-associated mRNA from complex tissues. Proc Natl Acad Sci USA 106(33):13939–13944CrossRefPubMedPubMedCentral
go back to reference Sarinana J, Kitamura T, Kunzler P, Sultzman L, Tonegawa S (2014) Differential roles of the dopamine 1-class receptors, D1R and D5R, in hippocampal dependent memory. Proc Natl Acad Sci USA 111(22):8245–8250CrossRefPubMedPubMedCentral Sarinana J, Kitamura T, Kunzler P, Sultzman L, Tonegawa S (2014) Differential roles of the dopamine 1-class receptors, D1R and D5R, in hippocampal dependent memory. Proc Natl Acad Sci USA 111(22):8245–8250CrossRefPubMedPubMedCentral
go back to reference Schultz W (2016) Dopamine reward prediction-error signalling: a two-component response. Nat Rev Neurosci 17(3):183–195CrossRefPubMed Schultz W (2016) Dopamine reward prediction-error signalling: a two-component response. Nat Rev Neurosci 17(3):183–195CrossRefPubMed
go back to reference Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9(1–6):321–353CrossRefPubMed Swanson LW (1982) The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9(1–6):321–353CrossRefPubMed
go back to reference Tricoire L, Pelkey KA, Daw MI, Sousa VH, Miyoshi G, Jeffries B, Cauli B, Fishell G, McBain CJ (2010) Common origins of hippocampal Ivy and nitric oxide synthase expressing neurogliaform cells. J Neurosci 30(6):2165–2176CrossRefPubMedPubMedCentral Tricoire L, Pelkey KA, Daw MI, Sousa VH, Miyoshi G, Jeffries B, Cauli B, Fishell G, McBain CJ (2010) Common origins of hippocampal Ivy and nitric oxide synthase expressing neurogliaform cells. J Neurosci 30(6):2165–2176CrossRefPubMedPubMedCentral
go back to reference Tricoire L, Pelkey KA, Erkkila BE, Jeffries BW, Yuan X, McBain CJ (2011) A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J Neurosci 31(30):10948–10970CrossRefPubMedPubMedCentral Tricoire L, Pelkey KA, Erkkila BE, Jeffries BW, Yuan X, McBain CJ (2011) A blueprint for the spatiotemporal origins of mouse hippocampal interneuron diversity. J Neurosci 31(30):10948–10970CrossRefPubMedPubMedCentral
go back to reference Valjent E, Bertran-Gonzalez J, Herve D, Fisone G, Girault JA (2009) Looking BAC at striatal signaling: cell-specific analysis in new transgenic mice. Trends Neurosci 32(10):538–547CrossRefPubMed Valjent E, Bertran-Gonzalez J, Herve D, Fisone G, Girault JA (2009) Looking BAC at striatal signaling: cell-specific analysis in new transgenic mice. Trends Neurosci 32(10):538–547CrossRefPubMed
go back to reference Walling SG, Brown RA, Miyasaka N, Yoshihara Y, Harley CW (2012) Selective wheat germ agglutinin (WGA) uptake in the hippocampus from the locus coeruleus of dopamine-beta-hydroxylase-WGA transgenic mice. Front Behav Neurosci 6:23CrossRefPubMedPubMedCentral Walling SG, Brown RA, Miyasaka N, Yoshihara Y, Harley CW (2012) Selective wheat germ agglutinin (WGA) uptake in the hippocampus from the locus coeruleus of dopamine-beta-hydroxylase-WGA transgenic mice. Front Behav Neurosci 6:23CrossRefPubMedPubMedCentral
go back to reference Wheeler DW, White CM, Rees CL, Komendantov AO, Hamilton DJ, Ascoli GA (2015) Hippocampome.org: a knowledge base of neuron types in the rodent hippocampus. Elife 4. doi:10.7554/eLife.09960 Wheeler DW, White CM, Rees CL, Komendantov AO, Hamilton DJ, Ascoli GA (2015) Hippocampome.org: a knowledge base of neuron types in the rodent hippocampus. Elife 4. doi:10.​7554/​eLife.​09960
Metadata
Title
Anatomical and molecular characterization of dopamine D1 receptor-expressing neurons of the mouse CA1 dorsal hippocampus
Authors
Emma Puighermanal
Laura Cutando
Jihane Boubaker-Vitre
Eve Honoré
Sophie Longueville
Denis Hervé
Emmanuel Valjent
Publication date
01-05-2017
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 4/2017
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1314-x

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