Skip to main content
Erschienen in: Brain Structure and Function 5/2017

03.12.2016 | Original Article

NR2A- and NR2B-NMDA receptors and drebrin within postsynaptic spines of the hippocampus correlate with hunger-evoked exercise

verfasst von: Yi-Wen Chen, Hannah Actor-Engel, Ang Doma Sherpa, Lauren Klingensmith, Tara G. Chowdhury, Chiye Aoki

Erschienen in: Brain Structure and Function | Ausgabe 5/2017

Einloggen, um Zugang zu erhalten

Abstract

Hunger evokes foraging. This innate response can be quantified as voluntary wheel running following food restriction (FR). Paradoxically, imposing severe FR evokes voluntary FR, as some animals choose to run rather than eat, even during limited periods of food availability. This phenomenon, called activity-based anorexia (ABA), has been used to identify brain changes associated with FR and excessive exercise (EX), two core symptoms of anorexia nervosa (AN), and to explore neurobiological bases of AN vulnerability. Previously, we showed a strong positive correlation between suppression of FR-evoked hyperactivity, i.e., ABA resilience, and levels of extra-synaptic GABA receptors in stratum radiatum (SR) of hippocampal CA1. Here, we tested for the converse: whether animals with enhanced expression of NMDA receptors (NMDARs) exhibit greater levels of FR-evoked hyperactivity, i.e., ABA vulnerability. Four groups of animals were assessed for NMDAR levels at CA1 spines: (1) ABA, in which 4 days of FR was combined with wheel access to allow voluntary EX; (2) FR only; (3) EX only; and (4) control (CON) that experienced neither EX nor FR. Electron microscopy revealed that synaptic NR2A-NMDARs and NR2B-NMDARs levels are significantly elevated, relative to CONs’. Individuals’ ABA severity, based on weight loss, correlated with synaptic NR2B-NMDAR levels. ABA resilience, quantified as suppression of hyperactivity, correlated strongly with reserve pools of NR2A-NMDARs in spine cytoplasm. NR2A- and NR2B-NMDAR measurements correlated with spinous prevalence of an F-actin binding protein, drebrin, suggesting that drebrin enables insertion of NR2B-NMDAR to and retention of NR2A-NMDARs away from synaptic membranes, together influencing ABA vulnerability.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
Zurück zum Zitat Adams MM, Fink SE, Janssen WG, Shah RA, Morrison JH (2004) Estrogen modulates synaptic N-methyl-D-aspartate receptor subunit distribution in the aged hippocampus. J Comp Neurol 474(3):419–426. doi:10.1002/cne.20148 CrossRefPubMed Adams MM, Fink SE, Janssen WG, Shah RA, Morrison JH (2004) Estrogen modulates synaptic N-methyl-D-aspartate receptor subunit distribution in the aged hippocampus. J Comp Neurol 474(3):419–426. doi:10.​1002/​cne.​20148 CrossRefPubMed
Zurück zum Zitat Aoki C, Erisir A (2014) Experience-dependent synaptic plasticity in the developing cerebral cortex. In: Segal M, Pickel VM (eds.) The Synapse: Structure and Function, vol 3. Neuroscience-Net Reference Book Series, 1st edn. Academic Press, Elsevier, pp 397–446 Aoki C, Erisir A (2014) Experience-dependent synaptic plasticity in the developing cerebral cortex. In: Segal M, Pickel VM (eds.) The Synapse: Structure and Function, vol 3. Neuroscience-Net Reference Book Series, 1st edn. Academic Press, Elsevier, pp 397–446
Zurück zum Zitat Aoki C, Carlin RK, Siekevitz P (1985) Comparison of proteins involved with cyclic AMP metabolism between synaptic membrane and postsynaptic density preparations isolated from canine cerebral cortex and cerebellum. J Neurochem 44(3):966–978CrossRefPubMed Aoki C, Carlin RK, Siekevitz P (1985) Comparison of proteins involved with cyclic AMP metabolism between synaptic membrane and postsynaptic density preparations isolated from canine cerebral cortex and cerebellum. J Neurochem 44(3):966–978CrossRefPubMed
Zurück zum Zitat Aoki C, Rodrigues S, Kurose H (2000) Use of electron microscopy in the detection of adrenergic receptors. Methods Mol Biol 126:535–563PubMedPubMedCentral Aoki C, Rodrigues S, Kurose H (2000) Use of electron microscopy in the detection of adrenergic receptors. Methods Mol Biol 126:535–563PubMedPubMedCentral
Zurück zum Zitat Aoki C, Fujisawa S, Mahadomrongkul V, Shah PJ, Nader K, Erisir A (2003) NMDA receptor blockade in intact adult cortex increases trafficking of NR2A subunits into spines, postsynaptic densities, and axon terminals. Brain Res 963(1–2):139–149CrossRefPubMed Aoki C, Fujisawa S, Mahadomrongkul V, Shah PJ, Nader K, Erisir A (2003) NMDA receptor blockade in intact adult cortex increases trafficking of NR2A subunits into spines, postsynaptic densities, and axon terminals. Brain Res 963(1–2):139–149CrossRefPubMed
Zurück zum Zitat Aoki C, Sekino Y, Hanamura K, Fujisawa S, Mahadomrongkul V, Ren Y, Shirao T (2005) Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses. J Comp Neurol 483(4):383–402. doi:10.1002/cne.20449 CrossRefPubMed Aoki C, Sekino Y, Hanamura K, Fujisawa S, Mahadomrongkul V, Ren Y, Shirao T (2005) Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses. J Comp Neurol 483(4):383–402. doi:10.​1002/​cne.​20449 CrossRefPubMed
Zurück zum Zitat Aoki C, Mahadomrongkul V, Fujisawa S, Habersat R, Shirao T (2007) Chemical and morphological alterations of spines within the hippocampus and entorhinal cortex precede the onset of Alzheimer’s disease pathology in double knock-in mice. J Comp Neurol 505(4):352–362. doi:10.1002/cne.21485 CrossRefPubMedPubMedCentral Aoki C, Mahadomrongkul V, Fujisawa S, Habersat R, Shirao T (2007) Chemical and morphological alterations of spines within the hippocampus and entorhinal cortex precede the onset of Alzheimer’s disease pathology in double knock-in mice. J Comp Neurol 505(4):352–362. doi:10.​1002/​cne.​21485 CrossRefPubMedPubMedCentral
Zurück zum Zitat Aoki C, Kojima N, Sabaliauskas N, Shah L, Ahmed TH, Oakford J, Ahmed T, Yamazaki H, Hanamura K, Shirao T (2009a) Drebrin a knockout eliminates the rapid form of homeostatic synaptic plasticity at excitatory synapses of intact adult cerebral cortex. J Comp Neurol 517(1):105–121CrossRefPubMedPubMedCentral Aoki C, Kojima N, Sabaliauskas N, Shah L, Ahmed TH, Oakford J, Ahmed T, Yamazaki H, Hanamura K, Shirao T (2009a) Drebrin a knockout eliminates the rapid form of homeostatic synaptic plasticity at excitatory synapses of intact adult cerebral cortex. J Comp Neurol 517(1):105–121CrossRefPubMedPubMedCentral
Zurück zum Zitat Aoki C, Lee J, Nedelescu H, Ahmed T, Ho A, Shen J (2009b) Increased levels of NMDA receptor NR2A subunits at pre- and postsynaptic sites of the hippocampal CA1: An early response to conditional double knockout of presenilin 1 and 2. J Comp Neurol 517(4):512–523CrossRefPubMedPubMedCentral Aoki C, Lee J, Nedelescu H, Ahmed T, Ho A, Shen J (2009b) Increased levels of NMDA receptor NR2A subunits at pre- and postsynaptic sites of the hippocampal CA1: An early response to conditional double knockout of presenilin 1 and 2. J Comp Neurol 517(4):512–523CrossRefPubMedPubMedCentral
Zurück zum Zitat Aoki C, Sabaliauskas N, Chowdhury T, Min JY, Colacino AR, Laurino K, Barbarich-Marsteller NC (2012) Adolescent female rats exhibiting activity-based anorexia express elevated levels of GABA(A) receptor alpha4 and delta subunits at the plasma membrane of hippocampal CA1 spines. Synapse 66(5):391–407. doi:10.1002/syn.21528 CrossRefPubMedPubMedCentral Aoki C, Sabaliauskas N, Chowdhury T, Min JY, Colacino AR, Laurino K, Barbarich-Marsteller NC (2012) Adolescent female rats exhibiting activity-based anorexia express elevated levels of GABA(A) receptor alpha4 and delta subunits at the plasma membrane of hippocampal CA1 spines. Synapse 66(5):391–407. doi:10.​1002/​syn.​21528 CrossRefPubMedPubMedCentral
Zurück zum Zitat Aoki C, Chowdhury TG, Wable GS, Chen YW (2016) Synaptic changes in the hippocampus of adolescent female rodents associated with resilience to anxiety and suppression of food restriction-evoked hyperactivity in an animal model for anorexia nervosa. Brain Res. doi:10.1016/j.brainres.2016.01.019 Aoki C, Chowdhury TG, Wable GS, Chen YW (2016) Synaptic changes in the hippocampus of adolescent female rodents associated with resilience to anxiety and suppression of food restriction-evoked hyperactivity in an animal model for anorexia nervosa. Brain Res. doi:10.​1016/​j.​brainres.​2016.​01.​019
Zurück zum Zitat Bachner-Melman R, Lerer E, Zohar AH, Kremer I, Elizur Y, Nemanov L, Golan M, Blank S, Gritsenko I, Ebstein RP (2007) Anorexia nervosa, perfectionism, and dopamine D4 receptor (DRD4). Am J Med Genet B Neuropsychiatr Genet 144B(6):748–756. doi:10.1002/ajmg.b.30505 CrossRefPubMed Bachner-Melman R, Lerer E, Zohar AH, Kremer I, Elizur Y, Nemanov L, Golan M, Blank S, Gritsenko I, Ebstein RP (2007) Anorexia nervosa, perfectionism, and dopamine D4 receptor (DRD4). Am J Med Genet B Neuropsychiatr Genet 144B(6):748–756. doi:10.​1002/​ajmg.​b.​30505 CrossRefPubMed
Zurück zum Zitat Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35(2):345–353CrossRefPubMed Barria A, Malinow R (2002) Subunit-specific NMDA receptor trafficking to synapses. Neuron 35(2):345–353CrossRefPubMed
Zurück zum Zitat Beals KA (2004) Disordered eating among athletes: a comprehensive guide for health professionals. Human Kinetic, Champagne Beals KA (2004) Disordered eating among athletes: a comprehensive guide for health professionals. Human Kinetic, Champagne
Zurück zum Zitat Boraska V, Franklin CS, Floyd JA, Thornton LM, Huckins LM, Southam L, Rayner NW, Tachmazidou I, Klump KL, Treasure J, Lewis CM, Schmidt U, Tozzi F, Kiezebrink K, Hebebrand J, Gorwood P, Adan RA, Kas MJ, Favaro A, Santonastaso P, Fernandez-Aranda F, Gratacos M, Rybakowski F, Dmitrzak-Weglarz M, Kaprio J, Keski-Rahkonen A, Raevuori A, Van Furth EF, Slof-Opt Landt MC, Hudson JI, Reichborn-Kjennerud T, Knudsen GP, Monteleone P, Kaplan AS, Karwautz A, Hakonarson H, Berrettini WH, Guo Y, Li D, Schork NJ, Komaki G, Ando T, Inoko H, Esko T, Fischer K, Mannik K, Metspalu A, Baker JH, Cone RD, Dackor J, Desocio JE, Hilliard CE, O’Toole JK, Pantel J, Szatkiewicz JP, Taico C, Zerwas S, Trace SE, Davis OS, Helder S, Buhren K, Burghardt R, de Zwaan M, Egberts K, Ehrlich S, Herpertz-Dahlmann B, Herzog W, Imgart H, Scherag A, Scherag S, Zipfel S, Boni C, Ramoz N, Versini A, Brandys MK, Danner UN, de Kovel C, Hendriks J, Koeleman BP, Ophoff RA, Strengman E, van Elburg AA, Bruson A, Clementi M, Degortes D, Forzan M, Tenconi E, Docampo E, Escaramis G, Jimenez-Murcia S, Lissowska J, Rajewski A, Szeszenia-Dabrowska N, Slopien A, Hauser J, Karhunen L, Meulenbelt I, Slagboom PE, Tortorella A, Maj M, Dedoussis G, Dikeos D, Gonidakis F, Tziouvas K, Tsitsika A, Papezova H, Slachtova L, Martaskova D, Kennedy JL, Levitan RD, Yilmaz Z, Huemer J, Koubek D, Merl E, Wagner G, Lichtenstein P, Breen G, Cohen-Woods S, Farmer A, McGuffin P, Cichon S, Giegling I, Herms S, Rujescu D, Schreiber S, Wichmann HE, Dina C, Sladek R, Gambaro G, Soranzo N, Julia A, Marsal S, Rabionet R, Gaborieau V, Dick DM, Palotie A, Ripatti S, Widen E, Andreassen OA, Espeseth T, Lundervold A, Reinvang I, Steen VM, Le Hellard S, Mattingsdal M, Ntalla I, Bencko V, Foretova L, Janout V, Navratilova M, Gallinger S, Pinto D, Scherer SW, Aschauer H, Carlberg L, Schosser A, Alfredsson L, Ding B, Klareskog L, Padyukov L, Courtet P, Guillaume S, Jaussent I, Finan C, Kalsi G, Roberts M, Logan DW, Peltonen L, Ritchie GR, Barrett JC, The Wellcome Trust Case Control C, Estivill X, Hinney A, Sullivan PF, Collier DA, Zeggini E, Bulik CM (2014) A genome-wide association study of anorexia nervosa. Mol Psychiatry. doi:10.1038/mp.2013.187 PubMedPubMedCentral Boraska V, Franklin CS, Floyd JA, Thornton LM, Huckins LM, Southam L, Rayner NW, Tachmazidou I, Klump KL, Treasure J, Lewis CM, Schmidt U, Tozzi F, Kiezebrink K, Hebebrand J, Gorwood P, Adan RA, Kas MJ, Favaro A, Santonastaso P, Fernandez-Aranda F, Gratacos M, Rybakowski F, Dmitrzak-Weglarz M, Kaprio J, Keski-Rahkonen A, Raevuori A, Van Furth EF, Slof-Opt Landt MC, Hudson JI, Reichborn-Kjennerud T, Knudsen GP, Monteleone P, Kaplan AS, Karwautz A, Hakonarson H, Berrettini WH, Guo Y, Li D, Schork NJ, Komaki G, Ando T, Inoko H, Esko T, Fischer K, Mannik K, Metspalu A, Baker JH, Cone RD, Dackor J, Desocio JE, Hilliard CE, O’Toole JK, Pantel J, Szatkiewicz JP, Taico C, Zerwas S, Trace SE, Davis OS, Helder S, Buhren K, Burghardt R, de Zwaan M, Egberts K, Ehrlich S, Herpertz-Dahlmann B, Herzog W, Imgart H, Scherag A, Scherag S, Zipfel S, Boni C, Ramoz N, Versini A, Brandys MK, Danner UN, de Kovel C, Hendriks J, Koeleman BP, Ophoff RA, Strengman E, van Elburg AA, Bruson A, Clementi M, Degortes D, Forzan M, Tenconi E, Docampo E, Escaramis G, Jimenez-Murcia S, Lissowska J, Rajewski A, Szeszenia-Dabrowska N, Slopien A, Hauser J, Karhunen L, Meulenbelt I, Slagboom PE, Tortorella A, Maj M, Dedoussis G, Dikeos D, Gonidakis F, Tziouvas K, Tsitsika A, Papezova H, Slachtova L, Martaskova D, Kennedy JL, Levitan RD, Yilmaz Z, Huemer J, Koubek D, Merl E, Wagner G, Lichtenstein P, Breen G, Cohen-Woods S, Farmer A, McGuffin P, Cichon S, Giegling I, Herms S, Rujescu D, Schreiber S, Wichmann HE, Dina C, Sladek R, Gambaro G, Soranzo N, Julia A, Marsal S, Rabionet R, Gaborieau V, Dick DM, Palotie A, Ripatti S, Widen E, Andreassen OA, Espeseth T, Lundervold A, Reinvang I, Steen VM, Le Hellard S, Mattingsdal M, Ntalla I, Bencko V, Foretova L, Janout V, Navratilova M, Gallinger S, Pinto D, Scherer SW, Aschauer H, Carlberg L, Schosser A, Alfredsson L, Ding B, Klareskog L, Padyukov L, Courtet P, Guillaume S, Jaussent I, Finan C, Kalsi G, Roberts M, Logan DW, Peltonen L, Ritchie GR, Barrett JC, The Wellcome Trust Case Control C, Estivill X, Hinney A, Sullivan PF, Collier DA, Zeggini E, Bulik CM (2014) A genome-wide association study of anorexia nervosa. Mol Psychiatry. doi:10.​1038/​mp.​2013.​187 PubMedPubMedCentral
Zurück zum Zitat Casper RC, Sullivan EL, Tecott L (2008) Relevance of animal models to human eating disorders and obesity. Psychopharmacol 199(3):313–329CrossRef Casper RC, Sullivan EL, Tecott L (2008) Relevance of animal models to human eating disorders and obesity. Psychopharmacol 199(3):313–329CrossRef
Zurück zum Zitat Chen YW, Wable GS, Chowdhury TG, Aoki C (2016) Enlargement of axo-somatic contacts formed by GAD-immunoreactive axon terminals onto layer V pyramidal neurons in the medial prefrontal cortex of adolescent female mice is associated with suppression of food restriction-evoked hyperactivity and resilience to activity-based anorexia. Cereb Cortex 26(6):2574–2589. doi:10.1093/cercor/bhv087 CrossRefPubMed Chen YW, Wable GS, Chowdhury TG, Aoki C (2016) Enlargement of axo-somatic contacts formed by GAD-immunoreactive axon terminals onto layer V pyramidal neurons in the medial prefrontal cortex of adolescent female mice is associated with suppression of food restriction-evoked hyperactivity and resilience to activity-based anorexia. Cereb Cortex 26(6):2574–2589. doi:10.​1093/​cercor/​bhv087 CrossRefPubMed
Zurück zum Zitat Chowdhury TG, Rios MB, Chan TE, Cassataro DS, Barbarich-Marsteller NC, Aoki C (2014b) Activity-based anorexia during adolescence disrupts normal development of the CA1 pyramidal cells in the ventral hippocampus of female rats. Hippocampus 24(12):1421–1429. doi:10.1002/hipo.22320 CrossRefPubMedPubMedCentral Chowdhury TG, Rios MB, Chan TE, Cassataro DS, Barbarich-Marsteller NC, Aoki C (2014b) Activity-based anorexia during adolescence disrupts normal development of the CA1 pyramidal cells in the ventral hippocampus of female rats. Hippocampus 24(12):1421–1429. doi:10.​1002/​hipo.​22320 CrossRefPubMedPubMedCentral
Zurück zum Zitat Chowdhury TG, Fenton AA, Aoki C (2014b) Adolescent experience of food restriction results in delayed enhancement of spatial learning in female rats. In: Paper presented at the Annual Meeting of the Society for Neuroscience, Washington, D.C Chowdhury TG, Fenton AA, Aoki C (2014b) Adolescent experience of food restriction results in delayed enhancement of spatial learning in female rats. In: Paper presented at the Annual Meeting of the Society for Neuroscience, Washington, D.C
Zurück zum Zitat Davis C, Katzman DK, Kaptein S, Kirsh C, Brewer H, Kalmbach K, Olmsted MP, Woodside DB, Kaplan AS (1997) The prevalence of high-level exercise in the eating disorders: etiological implications. Compr Psychiatry 38(6):321–326CrossRefPubMed Davis C, Katzman DK, Kaptein S, Kirsh C, Brewer H, Kalmbach K, Olmsted MP, Woodside DB, Kaplan AS (1997) The prevalence of high-level exercise in the eating disorders: etiological implications. Compr Psychiatry 38(6):321–326CrossRefPubMed
Zurück zum Zitat Dura JR, Bornstein RA (1989) Differences between IQ and school achievement in anorexia nervosa. J Clin Psychol 45(3):433–435CrossRefPubMed Dura JR, Bornstein RA (1989) Differences between IQ and school achievement in anorexia nervosa. J Clin Psychol 45(3):433–435CrossRefPubMed
Zurück zum Zitat Fujisawa S, Aoki C (2003) In vivo blockade of N-methyl-D-aspartate receptors induces rapid trafficking of NR2B subunits away from synapses and out of spines and terminals in adult cortex. Neuroscience 121(1):51–63CrossRefPubMedPubMedCentral Fujisawa S, Aoki C (2003) In vivo blockade of N-methyl-D-aspartate receptors induces rapid trafficking of NR2B subunits away from synapses and out of spines and terminals in adult cortex. Neuroscience 121(1):51–63CrossRefPubMedPubMedCentral
Zurück zum Zitat Fuss J, Ben Abdallah NM, Vogt MA, Touma C, Pacifici PG, Palme R, Witzemann V, Hellweg R, Gass P (2010) Voluntary exercise induces anxiety-like behavior in adult C57BL/6 J mice correlating with hippocampal neurogenesis. Hippocampus 20(3):364–376. doi:10.1002/hipo.20634 PubMed Fuss J, Ben Abdallah NM, Vogt MA, Touma C, Pacifici PG, Palme R, Witzemann V, Hellweg R, Gass P (2010) Voluntary exercise induces anxiety-like behavior in adult C57BL/6 J mice correlating with hippocampal neurogenesis. Hippocampus 20(3):364–376. doi:10.​1002/​hipo.​20634 PubMed
Zurück zum Zitat Guisinger S (2003) Adapted to flee famine: adding an evolutionary perspective on anorexia nervosa. Psychol Rev 110(4):745–761CrossRefPubMed Guisinger S (2003) Adapted to flee famine: adding an evolutionary perspective on anorexia nervosa. Psychol Rev 110(4):745–761CrossRefPubMed
Zurück zum Zitat Gutierrez E (2013) A rat in the labyrinth of anorexia nervosa: contributions of the activity-based anorexia rodent model to the understanding of anorexia nervosa. Int J Eat Disord 46(4):289–301CrossRefPubMed Gutierrez E (2013) A rat in the labyrinth of anorexia nervosa: contributions of the activity-based anorexia rodent model to the understanding of anorexia nervosa. Int J Eat Disord 46(4):289–301CrossRefPubMed
Zurück zum Zitat Kaufman AM, Milnerwood AJ, Sepers MD, Coquinco A, She K, Wang L, Lee H, Craig AM, Cynader M, Raymond LA (2012) Opposing roles of synaptic and extrasynaptic NMDA receptor signaling in cocultured striatal and cortical neurons. J Neurosci 32(12):3992–4003. doi:10.1523/JNEUROSCI.4129-11.2012 CrossRefPubMed Kaufman AM, Milnerwood AJ, Sepers MD, Coquinco A, She K, Wang L, Lee H, Craig AM, Cynader M, Raymond LA (2012) Opposing roles of synaptic and extrasynaptic NMDA receptor signaling in cocultured striatal and cortical neurons. J Neurosci 32(12):3992–4003. doi:10.​1523/​JNEUROSCI.​4129-11.​2012 CrossRefPubMed
Zurück zum Zitat Kaye WH, Bulik CM, Thornton L, Barbarich N, Masters K (2004) Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am J Psychiatry 161(12):2215–2221CrossRefPubMed Kaye WH, Bulik CM, Thornton L, Barbarich N, Masters K (2004) Comorbidity of anxiety disorders with anorexia and bulimia nervosa. Am J Psychiatry 161(12):2215–2221CrossRefPubMed
Zurück zum Zitat Klump KL, Miller KB, Keel PK, McGue M, Iacono WG (2001) Genetic and environmental influences on anorexia nervosa syndromes in a population-based twin sample. Psychol Med 31(4):737–740CrossRefPubMed Klump KL, Miller KB, Keel PK, McGue M, Iacono WG (2001) Genetic and environmental influences on anorexia nervosa syndromes in a population-based twin sample. Psychol Med 31(4):737–740CrossRefPubMed
Zurück zum Zitat Kron L, Katz JL, Gorzynski G, Weiner H (1978) Hyperactivity in anorexia nervosa: a fundamental clinical feature. Compr Psychiatry 19(5):433–440CrossRefPubMed Kron L, Katz JL, Gorzynski G, Weiner H (1978) Hyperactivity in anorexia nervosa: a fundamental clinical feature. Compr Psychiatry 19(5):433–440CrossRefPubMed
Zurück zum Zitat Li YH, Wang J, Zhang G (2009) Presynaptic NR2B-containing NMDA autoreceptors mediate gluta-matergic synaptic transmission in the rat visual cortex. Curr Neurovasc Res 6(2):104–109CrossRefPubMed Li YH, Wang J, Zhang G (2009) Presynaptic NR2B-containing NMDA autoreceptors mediate gluta-matergic synaptic transmission in the rat visual cortex. Curr Neurovasc Res 6(2):104–109CrossRefPubMed
Zurück zum Zitat Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304(5673):1021–1024. doi:10.1126/science.1096615 CrossRefPubMed Liu L, Wong TP, Pozza MF, Lingenhoehl K, Wang Y, Sheng M, Auberson YP, Wang YT (2004) Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science 304(5673):1021–1024. doi:10.​1126/​science.​1096615 CrossRefPubMed
Zurück zum Zitat Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24(36):7821–7828. doi:10.1523/JNEUROSCI.1697-04.2004 CrossRefPubMed Massey PV, Johnson BE, Moult PR, Auberson YP, Brown MW, Molnar E, Collingridge GL, Bashir ZI (2004) Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J Neurosci 24(36):7821–7828. doi:10.​1523/​JNEUROSCI.​1697-04.​2004 CrossRefPubMed
Zurück zum Zitat McIlhinney RA, Philipps E, Le Bourdelles B, Grimwood S, Wafford K, Sandhu S, Whiting P (2003) Assembly of N-methyl-D-aspartate (NMDA) receptors. Biochem Soc Trans 31(Pt 4):865–868CrossRefPubMed McIlhinney RA, Philipps E, Le Bourdelles B, Grimwood S, Wafford K, Sandhu S, Whiting P (2003) Assembly of N-methyl-D-aspartate (NMDA) receptors. Biochem Soc Trans 31(Pt 4):865–868CrossRefPubMed
Zurück zum Zitat Nedelescu H, Chowdhury TG, Wable GS, Arbuthnott G, Aoki C (2016) Cerebellar sub-divisions differ in exercise-induced plasticity of noradrenergic axons and in their association with resilience to activity-based anorexia. Brain Struct Funct. doi:10.1007/s00429-016-1220-2 PubMedPubMedCentral Nedelescu H, Chowdhury TG, Wable GS, Arbuthnott G, Aoki C (2016) Cerebellar sub-divisions differ in exercise-induced plasticity of noradrenergic axons and in their association with resilience to activity-based anorexia. Brain Struct Funct. doi:10.​1007/​s00429-016-1220-2 PubMedPubMedCentral
Zurück zum Zitat Peters A, Palay SL, Webster Hd (1991) The fine structure of the nervous system: neurons and their supporting cells, 3rd edn. Oxford University, New York Peters A, Palay SL, Webster Hd (1991) The fine structure of the nervous system: neurons and their supporting cells, 3rd edn. Oxford University, New York
Zurück zum Zitat Phend KD, Rustioni A, Weinberg RJ (1995) An osmium-free method of epon embedment that preserves both ultrastructure and antigenicity for post-embedding immunocytochemistry. J Histochem Cytochem 43(3):283–292CrossRefPubMed Phend KD, Rustioni A, Weinberg RJ (1995) An osmium-free method of epon embedment that preserves both ultrastructure and antigenicity for post-embedding immunocytochemistry. J Histochem Cytochem 43(3):283–292CrossRefPubMed
Zurück zum Zitat Pitsikas N, Carli M, Fidecka S, Algeri S (1990) Effect of life-long hypocaloric diet on age-related changes in motor and cognitive behavior in a rat population. Neurobiol Aging 11(4):417–423CrossRefPubMed Pitsikas N, Carli M, Fidecka S, Algeri S (1990) Effect of life-long hypocaloric diet on age-related changes in motor and cognitive behavior in a rat population. Neurobiol Aging 11(4):417–423CrossRefPubMed
Zurück zum Zitat Shen H, Gong QH, Aoki C, Yuan M, Ruderman Y, Dattilo M, Williams K, Smith SS (2007) Reversal of neurosteroid effects at alpha4beta2delta GABAA receptors triggers anxiety at puberty. Nat Neurosci 10(4):469–477PubMedPubMedCentral Shen H, Gong QH, Aoki C, Yuan M, Ruderman Y, Dattilo M, Williams K, Smith SS (2007) Reversal of neurosteroid effects at alpha4beta2delta GABAA receptors triggers anxiety at puberty. Nat Neurosci 10(4):469–477PubMedPubMedCentral
Zurück zum Zitat Shen H, Sabaliauskas N, Sherpa A, Fenton AA, Stelzer A, Aoki C, Smith SS (2010) A critical role for alpha4betadelta GABAA receptors in shaping learning deficits at puberty in mice. Science 327(5972):1515–1518CrossRefPubMedPubMedCentral Shen H, Sabaliauskas N, Sherpa A, Fenton AA, Stelzer A, Aoki C, Smith SS (2010) A critical role for alpha4betadelta GABAA receptors in shaping learning deficits at puberty in mice. Science 327(5972):1515–1518CrossRefPubMedPubMedCentral
Zurück zum Zitat Steinhausen HC (2002) The outcome of anorexia nervosa in the 20th century. Am J Psychiatry 159(8):1284–1293CrossRefPubMed Steinhausen HC (2002) The outcome of anorexia nervosa in the 20th century. Am J Psychiatry 159(8):1284–1293CrossRefPubMed
Zurück zum Zitat Stranahan AM, Lee K, Martin B, Maudsley S, Golden E, Cutler RG, Mattson MP (2009) Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 19(10):951–961. doi:10.1002/hipo.20577 CrossRefPubMedPubMedCentral Stranahan AM, Lee K, Martin B, Maudsley S, Golden E, Cutler RG, Mattson MP (2009) Voluntary exercise and caloric restriction enhance hippocampal dendritic spine density and BDNF levels in diabetic mice. Hippocampus 19(10):951–961. doi:10.​1002/​hipo.​20577 CrossRefPubMedPubMedCentral
Zurück zum Zitat Tang YP, Wang H, Feng R, Kyin M, Tsien JZ (2001) Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology 41(6):779–790CrossRefPubMed Tang YP, Wang H, Feng R, Kyin M, Tsien JZ (2001) Differential effects of enrichment on learning and memory function in NR2B transgenic mice. Neuropharmacology 41(6):779–790CrossRefPubMed
Zurück zum Zitat Tovar KR, Westbrook GL (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19(10):4180–4188PubMed Tovar KR, Westbrook GL (1999) The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J Neurosci 19(10):4180–4188PubMed
Zurück zum Zitat Wade TD, Bulik CM, Neale M, Kendler KS (2000) Anorexia nervosa and major depression: shared genetic and environmental risk factors. Am J Psychiatry 157(3):469–471CrossRefPubMed Wade TD, Bulik CM, Neale M, Kendler KS (2000) Anorexia nervosa and major depression: shared genetic and environmental risk factors. Am J Psychiatry 157(3):469–471CrossRefPubMed
Zurück zum Zitat Williams K (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44(4):851–859PubMed Williams K (1993) Ifenprodil discriminates subtypes of the N-methyl-D-aspartate receptor: selectivity and mechanisms at recombinant heteromeric receptors. Mol Pharmacol 44(4):851–859PubMed
Zurück zum Zitat Yu BP, Masoro EJ, Murata I, Bertrand HA, Lynd FT (1982) Life span study of SPF Fischer 344 male rats fed ad libitum or restricted diets: longevity, growth, lean body mass and disease. J Gerontol 37(2):130–141CrossRefPubMed Yu BP, Masoro EJ, Murata I, Bertrand HA, Lynd FT (1982) Life span study of SPF Fischer 344 male rats fed ad libitum or restricted diets: longevity, growth, lean body mass and disease. J Gerontol 37(2):130–141CrossRefPubMed
Metadaten
Titel
NR2A- and NR2B-NMDA receptors and drebrin within postsynaptic spines of the hippocampus correlate with hunger-evoked exercise
verfasst von
Yi-Wen Chen
Hannah Actor-Engel
Ang Doma Sherpa
Lauren Klingensmith
Tara G. Chowdhury
Chiye Aoki
Publikationsdatum
03.12.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Brain Structure and Function / Ausgabe 5/2017
Print ISSN: 1863-2653
Elektronische ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-016-1341-7

Weitere Artikel der Ausgabe 5/2017

Brain Structure and Function 5/2017 Zur Ausgabe

Leitlinien kompakt für die Neurologie

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Neurologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.