Skip to main content
Top
Published in: Brain Structure and Function 3/2011

01-09-2011 | Original Article

Laminar distribution of neurotransmitter receptors in different reeler mouse brain regions

Authors: Christian M. Cremer, Joachim H. R. Lübke, Nicola Palomero-Gallagher, Karl Zilles

Published in: Brain Structure and Function | Issue 3/2011

Login to get access

Abstract

Mapping of multiple receptors of neurotransmitters provides insight into the spatial distribution of neurotransmission-relevant molecules in the cerebral cortex. During development, lack of reelin leads to impaired migration, disturbed lamination of the hippocampus and inverted neocortical layering. In the adult, reelin may regulate synaptic plasticity by modulating neurotransmitter receptor function. Using quantitative in vitro receptor autoradiography, different receptors, in particular, the binding site densities and laminar distribution of various glutamate, GABA, muscarinic and nicotinic acetylcholine, serotonin, dopamine and adenosine receptors, were analyzed in cortical and subcortical structures of reeler and wild-type brains. Differential changes in the laminar distribution, maximum binding capacity (B max) and regional density of neurotransmitter receptors were found in the reeler brain. A decrease of whole brain B max was found for adenosine A1 and GABAA receptors. In the forebrain, several binding sites were differentially up- or down-regulated (kainate, A1, benzodiazepine, 5-HT1, M2, α1 and α2). In the hippocampus, a significant decrease of GABAB, 5-HT1 and \( {\text{A}}_1^{\prime} \) receptors were observed. The density of M2 receptors increased, while other receptors remained unchanged. In the neocortex, some receptors demonstrated an obviously inverted laminar distribution (AMPA, kainate, NMDA, GABAB, 5-HT1, M1, M3, nAch), while the distribution of others (A1, GABAA, benzodiazepine, 5-HT2, muscarinic M2, adrenergic α1, α2) seemed to be less affected. Thus, the laminar receptor distribution is modulated by the developmental impairment and suggests and reflects partially the laminar inversion in reeler mice.
Appendix
Available only for authorised users
Literature
go back to reference Angevine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766–768PubMedCrossRef Angevine JB, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766–768PubMedCrossRef
go back to reference Beffert U, Weeber EJ, Morfini G, Ko J, Brady ST, Tsai LH, Sweatt JD, Herz J (2004) Reelin and cyclin-dependent kinase 5-dependent signals cooperate in regulating neuronal migration and synaptic transmission. J Neurosci 24:1897–1906PubMedCrossRef Beffert U, Weeber EJ, Morfini G, Ko J, Brady ST, Tsai LH, Sweatt JD, Herz J (2004) Reelin and cyclin-dependent kinase 5-dependent signals cooperate in regulating neuronal migration and synaptic transmission. J Neurosci 24:1897–1906PubMedCrossRef
go back to reference Beffert U, Weeber EJ, Durudas A, Qiu S, Masiulis I, Sweatt JD, Li WP, Adelmann G, Frotscher M, Hammer RE, Herz J (2005) Modulation of synaptic plasticity and memory by Reelin involves differential splicing of the lipoprotein receptor ApoER2. Neuron 47:567–579PubMedCrossRef Beffert U, Weeber EJ, Durudas A, Qiu S, Masiulis I, Sweatt JD, Li WP, Adelmann G, Frotscher M, Hammer RE, Herz J (2005) Modulation of synaptic plasticity and memory by Reelin involves differential splicing of the lipoprotein receptor ApoER2. Neuron 47:567–579PubMedCrossRef
go back to reference Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, Liu QY, Colton CA, Barker JL (1999) Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 19:4449–4461PubMed Behar TN, Scott CA, Greene CL, Wen X, Smith SV, Maric D, Liu QY, Colton CA, Barker JL (1999) Glutamate acting at NMDA receptors stimulates embryonic cortical neuronal migration. J Neurosci 19:4449–4461PubMed
go back to reference Berry M, Rogers AW (1965) The migration of neuroblasts in the developing cerebral cortex. J Anat 99:691–709PubMed Berry M, Rogers AW (1965) The migration of neuroblasts in the developing cerebral cortex. J Anat 99:691–709PubMed
go back to reference Botella-Lopez A, Burgaya F, Gavin R, Garcia-Ayllon MS, Gomez-Tortosa E, Pena-Casanova J, Urena JM, Del Rio JA, Blesa R, Soriano E, Saéz-Valero J (2006) Reelin expression and glycosylation patterns are altered in Alzheimer’s disease. Proc Natl Acad Sci USA 103:5573–5578PubMedCrossRef Botella-Lopez A, Burgaya F, Gavin R, Garcia-Ayllon MS, Gomez-Tortosa E, Pena-Casanova J, Urena JM, Del Rio JA, Blesa R, Soriano E, Saéz-Valero J (2006) Reelin expression and glycosylation patterns are altered in Alzheimer’s disease. Proc Natl Acad Sci USA 103:5573–5578PubMedCrossRef
go back to reference Caviness VS Jr (1982) Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res 256:293–302PubMed Caviness VS Jr (1982) Neocortical histogenesis in normal and reeler mice: a developmental study based upon [3H]thymidine autoradiography. Brain Res 256:293–302PubMed
go back to reference Caviness VS, Frost DO (1983) Thalamocortical projections in the reeler mutant mouse. J Comp Neurol 219:182–202PubMedCrossRef Caviness VS, Frost DO (1983) Thalamocortical projections in the reeler mutant mouse. J Comp Neurol 219:182–202PubMedCrossRef
go back to reference Caviness VS, Sidman RL (1973) Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice. An autoradiographic analysis. J Comp Neurol 148:141–151PubMedCrossRef Caviness VS, Sidman RL (1973) Time of origin or corresponding cell classes in the cerebral cortex of normal and reeler mutant mice. An autoradiographic analysis. J Comp Neurol 148:141–151PubMedCrossRef
go back to reference Chen Y, Beffert U, Ertunc M, Tang TS, Kavalali ET, Bezprozvanny I, Herz J (2005) Reelin modulates NMDA receptor activity in cortical neurons. J Neurosci 25:8209–8216PubMedCrossRef Chen Y, Beffert U, Ertunc M, Tang TS, Kavalali ET, Bezprozvanny I, Herz J (2005) Reelin modulates NMDA receptor activity in cortical neurons. J Neurosci 25:8209–8216PubMedCrossRef
go back to reference Chin J, Massaro CM, Palop JJ, Thwin MT, Yu GQ, Bien-Ly N, Bender A, Mucke L (2007) Reelin depletion in the entorhinal cortex of human amyloid precursor protein transgenic mice and humans with Alzheimer’s disease. J Neurosci 27:2727–2733PubMedCrossRef Chin J, Massaro CM, Palop JJ, Thwin MT, Yu GQ, Bien-Ly N, Bender A, Mucke L (2007) Reelin depletion in the entorhinal cortex of human amyloid precursor protein transgenic mice and humans with Alzheimer’s disease. J Neurosci 27:2727–2733PubMedCrossRef
go back to reference Cremer CM, Palomero-Gallagher N, Bidmon HJ, Schleicher A, Speckmann EJ, Zilles K (2009) Pentylenetetrazole-induced seizures affect binding site densities for GABA, glutamate and adenosine receptors in the rat brain. Neuroscience 163:490–499PubMedCrossRef Cremer CM, Palomero-Gallagher N, Bidmon HJ, Schleicher A, Speckmann EJ, Zilles K (2009) Pentylenetetrazole-induced seizures affect binding site densities for GABA, glutamate and adenosine receptors in the rat brain. Neuroscience 163:490–499PubMedCrossRef
go back to reference Cremer CM, Bidmon H-J, Görg B, Palomero-Gallagher N, Lopez Escobar J, Speckmann E-J, Zilles K (2010) Inhibition of glutamate/glutamine cycle in vivo results in decreased benzodiazepine binding and differentially regulated GABAergic subunit expression in the rat brain. Epilepsia 51(8):1446–1455 Cremer CM, Bidmon H-J, Görg B, Palomero-Gallagher N, Lopez Escobar J, Speckmann E-J, Zilles K (2010) Inhibition of glutamate/glutamine cycle in vivo results in decreased benzodiazepine binding and differentially regulated GABAergic subunit expression in the rat brain. Epilepsia 51(8):1446–1455
go back to reference D’Arcangelo G (2006) Reelin mouse mutants as models of cortical development disorders. Epilepsy Behav 8:81–90PubMedCrossRef D’Arcangelo G (2006) Reelin mouse mutants as models of cortical development disorders. Epilepsy Behav 8:81–90PubMedCrossRef
go back to reference D’Arcangelo G, Miao GG, Curran T (1996) Detection of the reelin breakpoint in reeler mice. Brain Res Mol Brain Res 39:234–236PubMedCrossRef D’Arcangelo G, Miao GG, Curran T (1996) Detection of the reelin breakpoint in reeler mice. Brain Res Mol Brain Res 39:234–236PubMedCrossRef
go back to reference de Bergeyck V, Nakajima K, Lambert de Rouvroit C, Naerhuyzen B, Goffinet AM, Miyata T, Ogawa M, Mikoshiba K (1997) A truncated Reelin protein is produced but not secreted in the ‘Orleans’ reeler mutation (Reln[rl-Orl]). Brain Res Mol Brain Res 50:85–90PubMedCrossRef de Bergeyck V, Nakajima K, Lambert de Rouvroit C, Naerhuyzen B, Goffinet AM, Miyata T, Ogawa M, Mikoshiba K (1997) A truncated Reelin protein is produced but not secreted in the ‘Orleans’ reeler mutation (Reln[rl-Orl]). Brain Res Mol Brain Res 50:85–90PubMedCrossRef
go back to reference Dekimoto H, Terashima T, Katsuyama Y (2010) Dispersion of the neurons expressing layer specific markers in the reeler brain. Dev Growth Differ 52:181–193PubMedCrossRef Dekimoto H, Terashima T, Katsuyama Y (2010) Dispersion of the neurons expressing layer specific markers in the reeler brain. Dev Growth Differ 52:181–193PubMedCrossRef
go back to reference Deutsch SI, Rosse RB, Lakshman RM (2006) Dysregulation of tau phosphorylation is a hypothesized point of convergence in the pathogenesis of Alzheimer’s disease, frontotemporal dementia and schizophrenia with therapeutic implications. Prog Neuropsychopharmacol Biol Psychiatry 30:1369–1380PubMedCrossRef Deutsch SI, Rosse RB, Lakshman RM (2006) Dysregulation of tau phosphorylation is a hypothesized point of convergence in the pathogenesis of Alzheimer’s disease, frontotemporal dementia and schizophrenia with therapeutic implications. Prog Neuropsychopharmacol Biol Psychiatry 30:1369–1380PubMedCrossRef
go back to reference Durakoglugil MS, Chen Y, White CL, Kavalali ET, Herz J (2009) Reelin signaling antagonizes beta-amyloid at the synapse. Proc Natl Acad Sci USA 106:15938–15943PubMedCrossRef Durakoglugil MS, Chen Y, White CL, Kavalali ET, Herz J (2009) Reelin signaling antagonizes beta-amyloid at the synapse. Proc Natl Acad Sci USA 106:15938–15943PubMedCrossRef
go back to reference Fatemi SH (2008) In: Reelin glycoprotein: structure, biology and roles in health and disease. Springer Science and Business Media, New York Fatemi SH (2008) In: Reelin glycoprotein: structure, biology and roles in health and disease. Springer Science and Business Media, New York
go back to reference Fredholm BB, Chen JF, Cunha RA, Svenningsson P, Vaugeois JM (2005a) Adenosine and brain function. Int Rev Neurobiol 63:191–270PubMedCrossRef Fredholm BB, Chen JF, Cunha RA, Svenningsson P, Vaugeois JM (2005a) Adenosine and brain function. Int Rev Neurobiol 63:191–270PubMedCrossRef
go back to reference Fredholm BB, Chen JF, Masino SA, Vaugeois JM (2005b) Actions of adenosine at its receptors in the CNS: insights from knockouts and drugs. Annu Rev Pharmacol Toxicol 45:385–412PubMedCrossRef Fredholm BB, Chen JF, Masino SA, Vaugeois JM (2005b) Actions of adenosine at its receptors in the CNS: insights from knockouts and drugs. Annu Rev Pharmacol Toxicol 45:385–412PubMedCrossRef
go back to reference Fukumitsu N, Ishii K, Kimura Y, Oda K, Hashimoto M, Suzuki M, Ishiwata K (2008) Adenosine A(1) receptors using 8-dicyclopropylmethyl-1-[(11)C]methyl-3-propylxanthine PET in Alzheimer’s disease. Ann Nucl Med 22:841–847PubMedCrossRef Fukumitsu N, Ishii K, Kimura Y, Oda K, Hashimoto M, Suzuki M, Ishiwata K (2008) Adenosine A(1) receptors using 8-dicyclopropylmethyl-1-[(11)C]methyl-3-propylxanthine PET in Alzheimer’s disease. Ann Nucl Med 22:841–847PubMedCrossRef
go back to reference Groc L, Choquet D, Stephenson FA, Verrier D, Manzoni OJ, Chavis P (2007) NMDA receptor surface trafficking and synaptic subunit composition are developmentally regulated by the extracellular matrix protein Reelin. J Neurosci 27:10165–10175PubMedCrossRef Groc L, Choquet D, Stephenson FA, Verrier D, Manzoni OJ, Chavis P (2007) NMDA receptor surface trafficking and synaptic subunit composition are developmentally regulated by the extracellular matrix protein Reelin. J Neurosci 27:10165–10175PubMedCrossRef
go back to reference Haas CA, Frotscher M (2010) Reelin deficiency causes granule cell dispersion in epilepsy. Exp Brain Res 200:141–149PubMedCrossRef Haas CA, Frotscher M (2010) Reelin deficiency causes granule cell dispersion in epilepsy. Exp Brain Res 200:141–149PubMedCrossRef
go back to reference Hack I, Hellwig S, Junghans D, Brunne B, Bock HH, Zhao S, Frotscher M (2007) Divergent roles of ApoER2 and Vldlr in the migration of cortical neurons. Development 134:3883–3891PubMedCrossRef Hack I, Hellwig S, Junghans D, Brunne B, Bock HH, Zhao S, Frotscher M (2007) Divergent roles of ApoER2 and Vldlr in the migration of cortical neurons. Development 134:3883–3891PubMedCrossRef
go back to reference Hamburgh M (1960) Observations on the neuropathology of “Reeler”, a neurological mutation in mice. Experientia 16:460–461CrossRef Hamburgh M (1960) Observations on the neuropathology of “Reeler”, a neurological mutation in mice. Experientia 16:460–461CrossRef
go back to reference Hamburgh M (1963) Analysis of the postnatal developmental effects of “reeler”, a neurological mutation in mice. A study in developmental genetics. Dev Biol 19:165–185PubMedCrossRef Hamburgh M (1963) Analysis of the postnatal developmental effects of “reeler”, a neurological mutation in mice. A study in developmental genetics. Dev Biol 19:165–185PubMedCrossRef
go back to reference Heinrich C, Nitta N, Flubacher A, Müller MC, Fahrner A, Kirsch M, Freiman T, Suzuki F, Depaulis A, Frotscher M, Haas CA (2006) Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J Neurosci 26:4701–4713PubMedCrossRef Heinrich C, Nitta N, Flubacher A, Müller MC, Fahrner A, Kirsch M, Freiman T, Suzuki F, Depaulis A, Frotscher M, Haas CA (2006) Reelin deficiency and displacement of mature neurons, but not neurogenesis, underlie the formation of granule cell dispersion in the epileptic hippocampus. J Neurosci 26:4701–4713PubMedCrossRef
go back to reference Howell BW, Hawkes R, Soriano P, Cooper JA (1997) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389:733–737PubMedCrossRef Howell BW, Hawkes R, Soriano P, Cooper JA (1997) Neuronal position in the developing brain is regulated by mouse disabled-1. Nature 389:733–737PubMedCrossRef
go back to reference Ikeda M, Mackay KB, Dewar D, McCulloch J (1993) Differential alterations in adenosine A1 and kappa 1 opioid receptors in the striatum in Alzheimer’s disease. Brain Res 616:211–217PubMedCrossRef Ikeda M, Mackay KB, Dewar D, McCulloch J (1993) Differential alterations in adenosine A1 and kappa 1 opioid receptors in the striatum in Alzheimer’s disease. Brain Res 616:211–217PubMedCrossRef
go back to reference Jaarsma D, Sebens JB, Korf J (1991) Reduction of adenosine A1-receptors in the perforant pathway terminal zone in Alzheimer hippocampus. Neurosci Lett 121:111–114PubMedCrossRef Jaarsma D, Sebens JB, Korf J (1991) Reduction of adenosine A1-receptors in the perforant pathway terminal zone in Alzheimer hippocampus. Neurosci Lett 121:111–114PubMedCrossRef
go back to reference Jansen KL, Faull RL, Dragunow M, Synek BL (1990) Alzheimer’s disease: changes in hippocampal N-methyl-D-aspartate, quisqualate, neurotensin, adenosine, benzodiazepine, serotonin and opioid receptors-an autoradiographic study. Neuroscience 39:613–627PubMedCrossRef Jansen KL, Faull RL, Dragunow M, Synek BL (1990) Alzheimer’s disease: changes in hippocampal N-methyl-D-aspartate, quisqualate, neurotensin, adenosine, benzodiazepine, serotonin and opioid receptors-an autoradiographic study. Neuroscience 39:613–627PubMedCrossRef
go back to reference Kalaria RN, Sromek S, Wilcox BJ, Unnerstall JR (1990) Hippocampal adenosine A1 receptors are decreased in Alzheimer’s disease. Neurosci Lett 118:257–260PubMedCrossRef Kalaria RN, Sromek S, Wilcox BJ, Unnerstall JR (1990) Hippocampal adenosine A1 receptors are decreased in Alzheimer’s disease. Neurosci Lett 118:257–260PubMedCrossRef
go back to reference Lambert de Rouvroit C, Goffinet AM (1998) The reeler mouse as a model of brain development. Adv Anat Embryol Cell Biol 150:1–106PubMed Lambert de Rouvroit C, Goffinet AM (1998) The reeler mouse as a model of brain development. Adv Anat Embryol Cell Biol 150:1–106PubMed
go back to reference Lopez-Bendito G, Molnar Z (2003) Thalamocortical development: how are we going to get there? Nat Rev Neurosci 4:276–289PubMedCrossRef Lopez-Bendito G, Molnar Z (2003) Thalamocortical development: how are we going to get there? Nat Rev Neurosci 4:276–289PubMedCrossRef
go back to reference Lopez-Bendito G, Lujan R, et al (2003) Blockade of GABA(B) receptors alters the tangential migration of cortical neurons. Cereb Cortex 13:932–942 Lopez-Bendito G, Lujan R, et al (2003) Blockade of GABA(B) receptors alters the tangential migration of cortical neurons. Cereb Cortex 13:932–942
go back to reference Lujan R, Shigemoto R, Lopez-Bendito G (2005) Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130:567–580PubMedCrossRef Lujan R, Shigemoto R, Lopez-Bendito G (2005) Glutamate and GABA receptor signalling in the developing brain. Neuroscience 130:567–580PubMedCrossRef
go back to reference Mariani J, Crepel F, Mikoshiba K, Changeux JP, Sotelo C (1977) Anatomical, physiological and biochemical studies of the cerebellum from Reeler mutant mouse. Philos Trans R Soc Lond B Biol Sci 281:1–28PubMedCrossRef Mariani J, Crepel F, Mikoshiba K, Changeux JP, Sotelo C (1977) Anatomical, physiological and biochemical studies of the cerebellum from Reeler mutant mouse. Philos Trans R Soc Lond B Biol Sci 281:1–28PubMedCrossRef
go back to reference Marrone MC, Marinelli S, Biamonte F, Keller F, Sgobio CA, Ammassari-Teule M, Bernardi G, Mercuri NB (2006) Altered cortico-striatal synaptic plasticity and related behavioural impairments in reeler mice. Eur J Neurosci 24:2061–2070PubMedCrossRef Marrone MC, Marinelli S, Biamonte F, Keller F, Sgobio CA, Ammassari-Teule M, Bernardi G, Mercuri NB (2006) Altered cortico-striatal synaptic plasticity and related behavioural impairments in reeler mice. Eur J Neurosci 24:2061–2070PubMedCrossRef
go back to reference Matsuzaki H, Minabe Y, Nakamura K, Suzuki K, Iwata Y, Sekine Y, Tsuchiya KJ, Sugihara G, Suda S, Takei N, Nakahara D, Hashimoto K, Nairn AC, Mori N, Sato K (2007) Disruption of reelin signaling attenuates methamphetamine-induced hyperlocomotion. Eur J Neurosci 25:3376–3384PubMedCrossRef Matsuzaki H, Minabe Y, Nakamura K, Suzuki K, Iwata Y, Sekine Y, Tsuchiya KJ, Sugihara G, Suda S, Takei N, Nakahara D, Hashimoto K, Nairn AC, Mori N, Sato K (2007) Disruption of reelin signaling attenuates methamphetamine-induced hyperlocomotion. Eur J Neurosci 25:3376–3384PubMedCrossRef
go back to reference Müller MC, Osswald M, Tinnes S, Haussler U, Jacobi A, Förster E, Frotscher M, Haas CA (2009) Exogenous reelin prevents granule cell dispersion in experimental epilepsy. Exp Neurol 216:390–397PubMedCrossRef Müller MC, Osswald M, Tinnes S, Haussler U, Jacobi A, Förster E, Frotscher M, Haas CA (2009) Exogenous reelin prevents granule cell dispersion in experimental epilepsy. Exp Neurol 216:390–397PubMedCrossRef
go back to reference Niu S, Yabut O, D’Arcangelo G (2008) The Reelin signaling pathway promotes dendritic spine development in hippocampal neurons. J Neurosci 28:10339–10348PubMedCrossRef Niu S, Yabut O, D’Arcangelo G (2008) The Reelin signaling pathway promotes dendritic spine development in hippocampal neurons. J Neurosci 28:10339–10348PubMedCrossRef
go back to reference Palomero-Gallagher N, Bidmon H-J, Cremer M, Schleicher A, Kircheis G, Reifenberger G, Kostopoulos G, Häussinger D, Zilles K (2009) Neurotransmitter receptor imbalances in motor cortex and basal ganglia in hepatic encephalopathy. Cell Physiol Biochem 24:291–306PubMedCrossRef Palomero-Gallagher N, Bidmon H-J, Cremer M, Schleicher A, Kircheis G, Reifenberger G, Kostopoulos G, Häussinger D, Zilles K (2009) Neurotransmitter receptor imbalances in motor cortex and basal ganglia in hepatic encephalopathy. Cell Physiol Biochem 24:291–306PubMedCrossRef
go back to reference Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates.Second Edition. Academic Press, San Diego Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates.Second Edition. Academic Press, San Diego
go back to reference Prestwich SA, Forda SR, Dolphin AC (1987) Adenosine antagonists increase spontaneous and evoked transmitter release from neuronal cells in culture. Brain Res 405:130–139PubMedCrossRef Prestwich SA, Forda SR, Dolphin AC (1987) Adenosine antagonists increase spontaneous and evoked transmitter release from neuronal cells in culture. Brain Res 405:130–139PubMedCrossRef
go back to reference Qiu S, Zhao LF, Korwek KM, Weeber EJ (2006) Differential reelin-induced enhancement of NMDA and AMPA receptor activity in the adult hippocampus. J Neurosci 26:12943–12955PubMedCrossRef Qiu S, Zhao LF, Korwek KM, Weeber EJ (2006) Differential reelin-induced enhancement of NMDA and AMPA receptor activity in the adult hippocampus. J Neurosci 26:12943–12955PubMedCrossRef
go back to reference Rakic P, Caviness VS Jr (1995) Cortical development: view from neurological mutants two decades later. Neuron 14:1101–1104PubMedCrossRef Rakic P, Caviness VS Jr (1995) Cortical development: view from neurological mutants two decades later. Neuron 14:1101–1104PubMedCrossRef
go back to reference Saéz-Valero J, Fodero LR, Sjogren M, Andreasen N, Amici S, Gallai V, Vanderstichele H, Vanmechelen E, Parnetti L, Blennow K, Small DH (2003) Glycosylation of acetylcholinesterase and butyrylcholinesterase changes as a function of the duration of Alzheimer’s disease. J Neurosci Res 72:520–526PubMedCrossRef Saéz-Valero J, Fodero LR, Sjogren M, Andreasen N, Amici S, Gallai V, Vanderstichele H, Vanmechelen E, Parnetti L, Blennow K, Small DH (2003) Glycosylation of acetylcholinesterase and butyrylcholinesterase changes as a function of the duration of Alzheimer’s disease. J Neurosci Res 72:520–526PubMedCrossRef
go back to reference Sheldon M, Rice DS, D’Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389:730–733PubMedCrossRef Sheldon M, Rice DS, D’Arcangelo G, Yoneshima H, Nakajima K, Mikoshiba K, Howell BW, Cooper JA, Goldowitz D, Curran T (1997) Scrambler and yotari disrupt the disabled gene and produce a reeler-like phenotype in mice. Nature 389:730–733PubMedCrossRef
go back to reference Sheppard AM, Pearlman AL (1997) Abnormal reorganization of preplate neurons and their associated extracellular matrix: an early manifestation of altered neocortical development in the reeler mutant mouse. J Comp Neurol 378:173–179PubMedCrossRef Sheppard AM, Pearlman AL (1997) Abnormal reorganization of preplate neurons and their associated extracellular matrix: an early manifestation of altered neocortical development in the reeler mutant mouse. J Comp Neurol 378:173–179PubMedCrossRef
go back to reference Simmons PA, Pearlman AL (1983) Receptive-field properties of transcallosal visual cortical neurons in the normal and reeler mouse. J Neurophysiol 50:838–848PubMed Simmons PA, Pearlman AL (1983) Receptive-field properties of transcallosal visual cortical neurons in the normal and reeler mouse. J Neurophysiol 50:838–848PubMed
go back to reference Simmons PA, Lemmon V, Pearlman AL (1982) Afferent and efferent connections of the striate and extrastriate visual cortex of the normal and reeler mouse. J Comp Neurol 211:295–308PubMedCrossRef Simmons PA, Lemmon V, Pearlman AL (1982) Afferent and efferent connections of the striate and extrastriate visual cortex of the normal and reeler mouse. J Comp Neurol 211:295–308PubMedCrossRef
go back to reference Sinagra M, Verrier D, Frankova D, Korwek KM, Blahos J, Weeber EJ, Manzoni OJ, Chavis P (2005) Reelin, very-low-density lipoprotein receptor, and apolipoprotein E receptor 2 control somatic NMDA receptor composition during hippocampal maturation in vitro. J Neurosci 25:6127–6136PubMedCrossRef Sinagra M, Verrier D, Frankova D, Korwek KM, Blahos J, Weeber EJ, Manzoni OJ, Chavis P (2005) Reelin, very-low-density lipoprotein receptor, and apolipoprotein E receptor 2 control somatic NMDA receptor composition during hippocampal maturation in vitro. J Neurosci 25:6127–6136PubMedCrossRef
go back to reference Stanfield BB, Cowan WM (1979) The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185:393–422PubMedCrossRef Stanfield BB, Cowan WM (1979) The morphology of the hippocampus and dentate gyrus in normal and reeler mice. J Comp Neurol 185:393–422PubMedCrossRef
go back to reference Stone TW, Ceruti S, Abbracchio MP (2009) Adenosine receptors and neurological disease: neuroprotection and neurodegeneration. Handb Exp Pharmacol 193:535–587PubMedCrossRef Stone TW, Ceruti S, Abbracchio MP (2009) Adenosine receptors and neurological disease: neuroprotection and neurodegeneration. Handb Exp Pharmacol 193:535–587PubMedCrossRef
go back to reference Strazielle C, Hayzoun K, Derer M, Mariani J, Lalonde R (2006) Regional brain variations of cytochrome oxidase activity in Relnrl-orl mutant mice. J Neurosci Res 83:821–831PubMedCrossRef Strazielle C, Hayzoun K, Derer M, Mariani J, Lalonde R (2006) Regional brain variations of cytochrome oxidase activity in Relnrl-orl mutant mice. J Neurosci Res 83:821–831PubMedCrossRef
go back to reference Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS Jr (1999) Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 19:10357–10371PubMed Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS Jr (1999) Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 19:10357–10371PubMed
go back to reference Terashima T, Inoue K, Inoue Y, Mikoshiba K (1987) Thalamic connectivity of the primary motor cortex of normal and reeler mutant mice. J Comp Neurol 257:405–421PubMedCrossRef Terashima T, Inoue K, Inoue Y, Mikoshiba K (1987) Thalamic connectivity of the primary motor cortex of normal and reeler mutant mice. J Comp Neurol 257:405–421PubMedCrossRef
go back to reference Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97:689–701PubMedCrossRef Trommsdorff M, Gotthardt M, Hiesberger T, Shelton J, Stockinger W, Nimpf J, Hammer RE, Richardson JA, Herz J (1999) Reeler/disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97:689–701PubMedCrossRef
go back to reference Ułas J, Brunner LC, Nguyen L, Cotman CW (1993) Reduced density of adenosine A1 receptors and preserved coupling of adenosine A1 receptors to G proteins in Alzheimer hippocampus: a quantitative autoradiographic study. Neuroscience 52:843–854PubMedCrossRef Ułas J, Brunner LC, Nguyen L, Cotman CW (1993) Reduced density of adenosine A1 receptors and preserved coupling of adenosine A1 receptors to G proteins in Alzheimer hippocampus: a quantitative autoradiographic study. Neuroscience 52:843–854PubMedCrossRef
go back to reference Wagener RJ, Csaba D, Zhao S, Haas CA, Staiger JF (2010) The somatosensory cortex of reeler mutant mice show absent layering but intact formation and behavioral activation of columnar somatotopic maps. J Neurosci 30:15700–15709PubMedCrossRef Wagener RJ, Csaba D, Zhao S, Haas CA, Staiger JF (2010) The somatosensory cortex of reeler mutant mice show absent layering but intact formation and behavioral activation of columnar somatotopic maps. J Neurosci 30:15700–15709PubMedCrossRef
go back to reference Ware ML, Fox JW, Gonzalez JL, Davis NM, Lambert de Rouvroit C, Russo CJ, Chua SC Jr, Goffinet AM, Walsh CA (1997) Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse. Neuron 19:239–249PubMedCrossRef Ware ML, Fox JW, Gonzalez JL, Davis NM, Lambert de Rouvroit C, Russo CJ, Chua SC Jr, Goffinet AM, Walsh CA (1997) Aberrant splicing of a mouse disabled homolog, mdab1, in the scrambler mouse. Neuron 19:239–249PubMedCrossRef
go back to reference Weeber EJ, Beffert U, Jones C, Christian JM, Förster E, Sweatt JD, Herz J (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 277:39944–39952PubMedCrossRef Weeber EJ, Beffert U, Jones C, Christian JM, Förster E, Sweatt JD, Herz J (2002) Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning. J Biol Chem 277:39944–39952PubMedCrossRef
go back to reference Wirths O, Multhaup G, Czech C, Blanchard V, Tremp G, Pradier L, Beyreuther K, Bayer TA (2001) Reelin in plaques of beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 316:145–148PubMedCrossRef Wirths O, Multhaup G, Czech C, Blanchard V, Tremp G, Pradier L, Beyreuther K, Bayer TA (2001) Reelin in plaques of beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 316:145–148PubMedCrossRef
go back to reference Zhao S, Chai X, Förster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117–5125PubMedCrossRef Zhao S, Chai X, Förster E, Frotscher M (2004) Reelin is a positional signal for the lamination of dentate granule cells. Development 131:5117–5125PubMedCrossRef
go back to reference Zilles K, Amunts K (2009) Receptor mapping: architecture of the human cerebral cortex. Curr Opin Neurol 22:331–339PubMedCrossRef Zilles K, Amunts K (2009) Receptor mapping: architecture of the human cerebral cortex. Curr Opin Neurol 22:331–339PubMedCrossRef
go back to reference Zilles K, Qü MS, Kohling R, Speckmann EJ (1999) Ionotropic glutamate and GABA receptors in human epileptic neocortical tissue: quantitative in vitro receptor autoradiography. Neuroscience 94:1051–1061PubMedCrossRef Zilles K, Qü MS, Kohling R, Speckmann EJ (1999) Ionotropic glutamate and GABA receptors in human epileptic neocortical tissue: quantitative in vitro receptor autoradiography. Neuroscience 94:1051–1061PubMedCrossRef
go back to reference Zilles K, Schleicher A, Palomero-Gallagher N, Amunts K (2002) Quantitative analysis of cyto- and receptor architecture of the human brain. In: Toga AW, Mazziotta JC (eds) Brain mapping. The methods. Elsevier, Amsterdam, pp 573–602CrossRef Zilles K, Schleicher A, Palomero-Gallagher N, Amunts K (2002) Quantitative analysis of cyto- and receptor architecture of the human brain. In: Toga AW, Mazziotta JC (eds) Brain mapping. The methods. Elsevier, Amsterdam, pp 573–602CrossRef
go back to reference Zilles K, Palomero-Gallagher N, Schleicher A (2004) Transmitter receptors and functional anatomy of the cerebral cortex. J Anat 205:417–432PubMedCrossRef Zilles K, Palomero-Gallagher N, Schleicher A (2004) Transmitter receptors and functional anatomy of the cerebral cortex. J Anat 205:417–432PubMedCrossRef
Metadata
Title
Laminar distribution of neurotransmitter receptors in different reeler mouse brain regions
Authors
Christian M. Cremer
Joachim H. R. Lübke
Nicola Palomero-Gallagher
Karl Zilles
Publication date
01-09-2011
Publisher
Springer-Verlag
Published in
Brain Structure and Function / Issue 3/2011
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-011-0303-3

Other articles of this Issue 3/2011

Brain Structure and Function 3/2011 Go to the issue