Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor


N-Methyl-D-aspartate receptors (NMDARs) are involved in learning and memory processes in vertebrates and invertebrates. In Neohelice granulata, NMDARs are involved in the storage of associative memories (see references in text). The aim of this work was to characterize this type of glutamate receptor in Neohelice and to describe its distribution in the central nervous system (CNS). As a first step, a detailed study of the CNS of N. granulata was performed at the neuropil level, with special focus on one of the main structures involved in this type of memory, the supraesophageal ganglion, called central brain. The characterization of the NMDAR was achieved by identifying the essential subunit of these receptors, the NR1-like subunit. The NR1-like signals were found via western blot and immunohistochemistry techniques in each of the major ganglia: the eyestalk ganglia, the central brain, and the thoracic ganglion. Western blots yielded two bands for the crab NR1-like subunit, at ∼88 and ∼84 kDa. This subunit is present in all the major ganglia, and shows a strong localization in synaptosomal membranes. NMDARs are distributed throughout the majority of each ganglion but show prominent signal intensity in some distinguishable neuropils and neurons. This is the first general description of the N. granulata nervous system as a whole and the first study of NMDARs in the CNS of decapods. The preferential localization of the receptor in some neuropils and neurons indicates the presence of possible new targets for memory processing and storage. © 2012 Wiley Periodicals, Inc.


Documento: Artículo
Título:NMDA-like receptors in the nervous system of the crab Neohelice granulata: A neuroanatomical description
Autor:Hepp, Y.; Tano, M.C.; Pedreira, M.E.; Freudenthal, R.A.M.
Filiación:Laboratorio de Neurobiología de la Memoria, Facultad de Ciencias Exactas y Naturales, Dep. Fisiología y Biologia Molecular y Celular, Universidad de Buenos Aires, Ciudad Universitaria, Ciudad Autónoma de Buenos Aires, Argentina
Palabras clave:Decapod; Ganglion; Invertebrate; Neohelice granulata; Neuropil; NR1 subunit; n methyl dextro aspartic acid receptor; n methyl dextro aspartic acid receptor 1; animal tissue; article; cellular distribution; controlled study; crab; eyestalk ganglion; ganglion; immunohistochemistry; male; Neohelice granulata; neuroanatomy; neuropil; nonhuman; priority journal; protein localization; supraesophageal ganglion; synaptic membrane; thoracic ganglion; Western blotting; Animals; Brachyura; Central Nervous System; Male; Membrane Proteins; Neurons; Receptors, N-Methyl-D-Aspartate; Serotonin; Synaptosomes
Página de inicio:2279
Página de fin:2297
Título revista:Journal of Comparative Neurology
Título revista abreviado:J. Comp. Neurol.
CAS:Membrane Proteins; NR1 NMDA receptor; Receptors, N-Methyl-D-Aspartate; Serotonin, 50-67-9


  • Amano, H., Maruyama, I.N., Aversive olfactory learning and associative long-term memory in Caenorhabditis elegans (2011) Learn Mem, 18, pp. 654-665
  • Berón de Astrada, M., Tomsic, D., Physiology and morphology of visual movement detector neurons in a crab (Decapoda: Brachyura) (2002) J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 188, pp. 539-551
  • Bicker, G., Schäfer, S., Ottersen, O.P., Storm-Mathisen, J., Glutamate-like immunoreactivity in identified neuronal populations of insect nervous systems (1988) J Neurosci, 8, pp. 2108-2122
  • Bonasio, R., Zhang, G., Ye, C., Mutti, N.S., Fang, X., Qin, N., Donahue, G., Liebig, J., Genomic comparison of the ants Camponotus floridanus and Harpegnathos saltator (2010) Science, 329, pp. 1068-1071
  • Bond-Buckup, G., Fontoura, N.F., Marroni, N.P., Kucharski, L.C., (1991), O′carangueijo-Manual para o ensino prático de zoologia. Ed. da Universidade, Univerdidade Federal do Rio Grande do Sul; Brockie, P.J., Mellem, J.E., Hills, T., Madsen, D.M., Maricq, A.V., The C. elegans glutamate receptor subunit NMR-1 is required for slow NMDA-activated currents that regulate reversal frequency during locomotion (2001) Neuron, 31, pp. 617-630
  • Browing, K., Lukowiak, K., Ketamine inhibits long-term, but not intermediate-term memory formation in Lymnaea stagnalis (2008) Neuroscience, 155, pp. 613-625
  • Burgess, M.F., Derby, C.D., Two novel types of L-glutamate receptors with affinities for NMDA and L-cysteine in the olfactory organ of the Caribbean spiny lobster Panulirus argus (1997) Brain Res, 771, pp. 292-304
  • Cain, D.P., LTP, NMDA, genes and learning (1997) Curr Opin Neurobiol, 2, pp. 235-242
  • Carew, T.J., Behavioral neurobiology (2000) The cellular organization of natural behavior, , Sunderland, MA: Sinauer
  • Chiang, A.S., Liu, Y.C., Chiu, S.L., Hu, S.H., Huang, C.Y., Hsieh, C.H., Three-dimensional mapping of brain neuropils in the cockroach, Diploptera punctata (2001) J Comp Neurol, 440, pp. 1-11
  • Chiang, A.S., Pszczolkowski, M.A., Liu, H.P., Lin, S.C., Ionotropic glutamate receptors mediate juvenile hormone synthesis in the cockroach, Diploptera punctata (2002) Insect Biochem Mol Biol, 32, pp. 669-678
  • Cull-Candy, S., Brickley, S., Farrant, M., NMDA receptor subunits: diversity, development and disease (2001) Curr Opin Neurobiol, 11, pp. 327-335
  • Dale, N., Kandel, E.R., L-glutamate may be the fast excitatory transmitter of Aplysia sensory neurons (1993) Proc Natl Acad Sci U S A, 90, pp. 7163-7167
  • Dingledine, R., Borges, K., Bowie, D., Traynelis, S.F., The glutamate receptor ion channels (1999) Pharmacol Rev, 51, pp. 7-61
  • Federman, N., Fustiñana, M.S., Romano, A., Histone acetylation is recruited in consolidation as a molecular feature of stronger memories (2009) Learn Mem, 16, pp. 600-606
  • Federman, N., Fustiñana, M.S., Romano, A., Reconsolidation involves histone acetylation depending on the strength of the memory (2012) Neuroscience, 219, pp. 145-156
  • Feinstein, N., Parnas, D., Parnas, H., Dudel, J., Parnas, I., Functional and immunocytochemical identification of glutamate autoreceptors of an NMDA type in crayfish neuromuscular junction (1998) J Neurophysiol, 80, pp. 2893-2899
  • Feld, M., Dimant, B., Delorenzi, A., Coso, O., Romano, A., Phosphorylation of extra-nuclear ERK/MAPK is required for long-termmemory consolidation in the crab Chasmagnathus (2005) Behav Brain Res, 158, pp. 251-261
  • Fischbach, K.-F., Dittrich, A.P.M., The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure (1989) Cell Tissue Res, 258, pp. 441-475
  • Fletcher, E.L., Hack, I., Brandstätter, J.H., Wässle, H., Synaptic localization of NMDA receptor subunits in the rat retina (2000) J Comp Neurol, 420, pp. 98-112
  • Frenkel, L., Maldonado, H., Delorenzi, A., Memory strengthening by a real-life episode during reconsolidation: an outcome of water deprivation via brain angiotensin II (2005) Eur J Neurosci, 22, pp. 1757-1766
  • Frenkel, L., Dimant, B., Portiansky, E.L., Maldonado, H., Delorenzi, A., Both heat shock and water deprivation trigger Hsp70 expression in the olfactory lobe of the crab Chasmagnathus granulatus (2008) Neurosci Lett, 443, pp. 251-256
  • Frenkel, L., Dimant, B., Portiansky, E.L., Imboden, H., Maldonado, H., Delorenzi, A., Neuroanatomical distribution of angiotensin-II-like neuropeptide within the central nervous system of the crab Chasmagnathus; physiological changes triggered by water deprivation (2010) Cell Tissue Res, 341, pp. 181-195
  • Frenkel, L., Dimant, B., Suárez, L.D., Portiansky, E.L., Delorenzi, A., Food odor, visual danger stimulus, and retrieval of an aversive memory trigger heat shock protein HSP70 expression in the olfactory lobe of the crab Chasmagnathus granulatus (2012) Neuroscience, 201, pp. 239-251
  • Freudenthal, R., Locatelli, F., Hermitte, G., Maldonado, H., Delorenzi, A., Romano, A., NFκB-like DNA binding activity is enhanced after spaced training that induces long-term memory in the crab Chasmagnathus (1998) Neurosci Lett, 242, pp. 143-146
  • Furukawa, F., Grouaux, E., Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core (2003) EMBO J, 22, pp. 2873-2885
  • Fustiñana, M.S., Ariel, P., Federman, N., Freudenthal, R., Romano, A., Characterization of the beta amyloid precursor protein-like gene in the central nervous system of the crab Chasmagnathus. Expression during memory consolidation (2010) BMC Neurosci, 11, p. 109
  • Gallus, L., Ferrando, S., Gambardella, C., Diaspro, A., Bianchini, P., Faimali, M., Ramoino, P., Tagliafierro, G., NMDA R1 receptor distribution in the cyprid of Balanus amphitrite (=Amphibalanus amphitrite) (Cirripedia, Crustacea) (2010) Neurosci Lett, 485, pp. 183-188
  • Grey, K.B., Moss, B.L., Burrell, B.D., Molecular identification and expression of the NMDA receptor NR1 subunit in the leech (2009) Invert Neurosci, 9, pp. 11-20
  • Gutiérrez, H., Gutiérrez, R., Silva-Gandarias, R., Estrada, J., Miranda, M.I., Bermúdez-Rattoni, F., Differential effects of 192IgG-saporin and NMDA-induced lesions into the basal forebrain on cholinergic activity and taste aversion memory formation (1999) Brain Res, 834, pp. 136-141
  • Ha, T.J., Kohn, A.B., Bobkova, Y.V., Moroz, L.L., Molecular characterization of NMDA-like receptors in Aplysia and Lymnaea: relevance to memory mechanisms (2006) Biol Bull, 210, pp. 255-270
  • Harzsch, S., Neurophylogeny: architecture of the nervous system and a fresh view on arthropod phyologeny (2006) Integr Comp Biol, 46, pp. 162-194
  • Harzsch, S., Hansson, B.S., Brain architecture in the terrestrial hermit crab Coenobita clypeatus (Anomura, Coenobitidae), a crustacean with a good aerial sense of smell (2008) BMC Neurosci, 9, p. 58
  • Harzsch, S., Miller, J., Benton, J., Beltz, B., From embryo to adult: persistent neurogenesis and apoptotic cell death shape the lobster deutocerebrum (1999) J Neurosci, 19, pp. 3472-3485
  • Hepp, Y., Pérez-Cuesta, L.M., Maldonado, H., Pedreira, M.E., Extinction memory in the crab Chasmagnathus: recovery protocols and effects of multi-trial extinction training (2010) Anim Cogn, 13, pp. 391-403
  • Hollmann, M., Structure of ionotropic glutamate receptors (1999) Ionotropic glutamate receptors in the CNS, pp. 1-98. , Jonas P, Monyer H, editors. Berlin: Springer
  • Hollmann, M., Boulter, J., Maron, C., Beasley, L., Sullivan, J., Pecht, G., Heinemann, S., Zinc potentiates agonist-induced currents at certain splice variants of the NMDA receptor (1993) Neuron, 10, pp. 943-954
  • Homberg, U., Evolution of the central complex in the arthropod brain with respect to the visual system (2008) Arthropod Struct Dev, 37, pp. 347-362
  • Kano, T., Brockie, P.J., Sassa, T., Fujimoto, H., Kawahara, Y., Iino, Y., Mellem, J.E., Maricq, A.V., Memory in Caenorhabditis elegans is mediated by NMDA-type ionotropic glutamate receptors (2008) Curr Biol, 18, pp. 1010-1015
  • Klagges, B.R., Heimbeck, G., Godenschwege, T.A., Hofbauer, A., Pflugfelder, G.O., Reifegerste, R., Reisch, D., Buchner, E., Invertebrate synapsins: a single gene codes for several isoforms in Drosophila (1996) J Neurosci, 16, pp. 3154-3165
  • Krieger, J., Sandeman, R.E., Sandeman, D.C., Hansson, B.S., Harzsch, S., Brain architecture of the largest living land arthropod, the Giant Robber Crab Birgus latro (Crustacea, Anomura, Coenobitidae): evidence for a prominent central olfactory pathway? (2010) Front Zool, 7, p. 25
  • Krieger, J., Sombke, A., Seefluth, F., Kenning, M., Hansson, B.S., Harzsch, S., Comparative brain architecture of the European shore crab Carcinus maenas (Brachyura) and the common hermit crab Pagurus bernhardus (Anomura) with notes on other marine hermit crabs (2012) Cell Tissue Res, 348, pp. 47-69
  • Lin, X.Y., Glanzman, D.L., Hebbian induction of long-term potentiation of Aplysia sensorimotor synapses: partial requirement for activation of an NMDA-related receptor (1994) Proc Biol Sci, 255, pp. 215-221
  • Lin, X.Y., Glanzman, D.L., Effect of interstimulus interval on pairing-induced LTP of Aplysia sensorimotor synapses in cell culture (1997) J Neurophysiol, 77, pp. 667-674
  • Locatelli, F., Romano, A., Differential activity profile of cAMP-dependent protein kinase isoforms during long-term memory consolidation in the crab Chasmagnathus (2005) Neurobiol Learn Mem, 83, pp. 232-242
  • Maldonado, H., Crustaceans as models to investigate memory illustrated by extensive behavioral and physiological studies in Chasmagnathus (2002) The crustacean nervous system, pp. 314-327. , Wiese E, editor. Berlin: Springer
  • Mayer, M.L., Benveniste, M., Patneau, D.K., NMDA receptor agonists and competitive antagonists (1994) The NMDA receptor, pp. 132-146. , Collingridge GL, Watkins JC, editors., 2nd ed. New York: Oxford University Press
  • Maynard, D.R., Activity in a crustacean ganglion. I. Cardioinhibition and acceleration in Panulirus argus (1953) Biol Bull, 104, pp. 156-170
  • McBain, C.J., Mayer, M.L., N-methyl-D-aspartic acid receptor structure and function (1994) Physiol Rev, 74, pp. 723-760
  • McLaughlin, P.A., Internal anatomy (1983), 5, p. 41. , Bliss DE, editor, The biology of Crustacea, New York: Academic Press; Medan, V., Oliva, D., Tomsic, D., Characterization of lobula giant neurons responsive to visual stimuli that elicit escape behaviors in the crab Chasmagnathus (2007) J Neurophysiol, 98, pp. 2414-2428
  • Merlo, E., Romano, A., Long-term memory consolidation depends on proteasome activity in the crab Chasmagnathus (2007) Neuroscience, 147, pp. 46-52
  • Merlo, E., Romano, A., Memory extinction entails the inhibition of the transcription factor NF-kappaB (2008) PLoS One, 3, pp. e3687
  • Miserendino, M.J., Sananes, C.B., Melia, K.R., Davis, M., Blocking of acquisition but not expression on conditioned fear-potentiated startle by NMDA antagonists in the amygdala (1990) Nature, 345, pp. 716-718
  • Miyashita, T., Oda, Y., Horiuchi, J., Yin, J.C., Morimoto, T., Saitoe, M., Mg(2+) block of Drosophila NMDA receptors is required for long-term memory formation and CREB-dependent gene expression (2012) Neuron, 74, pp. 887-898
  • Moroz, L.L., Györi, J., Salánki, J., NMDA-like receptors in the CNS of molluscs (1993) Neuroreport, 4, pp. 201-204
  • Morris, R.G., Anderson, E., Lynch, G.S., Baudry, M., Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5 (1986) Nature, 319, pp. 774-776
  • Müβig, L., Richlitzki, A., Rössler, R., Eisenhardt, D., Menzel, R., Leboulle, G., Acute disruption of the NMDA receptor subunit NR1 in the honeybee brain selectively impairs memory formation (2010) J Neurosci, 30, pp. 7817-7825
  • Nässel, D.R., Elofsson, R., Comparative anatomy of the crustacean brain (1987) Arthropod brain, pp. 111-135. , Gupta AP, editor. New York: John Wiley & Sons
  • Papadakis, M., Hawkins, L.M., Stephenson, F.A., Appropriate NR1-NR1 disulfide-linked homodimer formation is requisite for efficient expression of functional, cell surface N-methyl-D-aspartate NR1/NR2 receptors (2004) J Biol Chem, 279, pp. 14703-14712
  • Parnas, H., Parnas, I., Ravin, R., Yudelevitch, B., Glutamate and N-methyl-D-aspartate affect release from crayfish axon terminals in a voltage-dependent manner (1994) Proc Natl Acad Sci U S A, 91, pp. 11586-11590
  • Parnas, I., Dudel, J., Parnas, H., Ravin, R., Glutamate depresses release by activating non-conventional glutamate receptors at crayfish nerve terminals (1996) Eur J Neurosci, 8, pp. 116-126
  • Pedreira, M.E., Maldonado, H., Protein synthesis subserves reconsolidation or extinction depending on reminder duration (2003) Neuron, 38, pp. 863-869
  • Pedreira, M.E., Pérez-Cuesta, L.M., Maldonado, H., Reactivation and reconsolidation of long-term memory in the crab Chasmagnathus: protein synthesis requirement and mediation by NMDA-type glutamatergic receptors (2002) J Neurosci, 32, pp. 8305-8311
  • Pérez-Cuesta, L.M., Maldonado, H., Memory reconsolidation and extinction in the crab: mutual exclusion or coexistence? (2009) Learn Mem, 16, pp. 714-721
  • Pérez-Cuesta, L.M., Hepp, Y., Pedreira, M.E., Maldonado, H., Extinction is not developed along with CS presentation but within a few seconds after CS-offset (2007) Learn Mem, 14, pp. 101-108
  • Petralia, R.S., Wang, Y.X., Wenthold, R.J., The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1 (1994) J Neurosci, 14, pp. 6102-6020
  • Pfeiffer-Linn, C., Glantz, R.M., An arthropod NMDA receptor (1991) Synapse, 9, pp. 35-42
  • Rao, A., Craig, A.M., Activity regulates the synaptic localization of the NMDA receptor in hippocampal neurons (1997) Neuron, 19, pp. 801-812
  • Richter, S., Loesel, R., Purschke, G., Schmidt-Rhaesa, A., Scholtz, G., Stach, T., Vogt, L., Harzsch, S., Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary (2010) Front Zool, 7, p. 29
  • Rickard, N.S., Poot, A.C., Gibbs, M.E., Ng, K.T., Both non-NMDA and NMDA glutamate receptors are necessary for memory consolidation in the day-old chick (1994) Behav Neural Biol, 62, pp. 33-40
  • Rieger, A.M., Hall, B.E., Luong le, T., Schang, L.M., Barreda, D.R., Conventional apoptosis assays using propidium iodide generate a significant number of false positives that prevent accurate assessment of cell death (2010) J Immunol Methods., 358, pp. 81-92
  • Roberts, A.C., Glanzman, D.L., Learning in Aplysia: looking at synaptic plasticity from both sides (2003) Trends Neurosci, 26, pp. 662-670
  • Romano, A., Locatelli, F., Freudenthal, R., Merlo, E., Feld, M., Ariel, P., Lemos, D., Fustiñana, M.S., Lessons from a crab: molecular mechanisms in different memory phases of Chasmagnathus (2006) Biol Bull, 210, pp. 280-288
  • Rosenegger, D., Lukowiak, K., The participation of NMDA receptors, PKC, and MAPK in the formation of memory following operant conditioning in Lymnaea (2010) Mol Brain, 3, p. 24
  • Sandeman, D.C., Organization of the central nervous system (1982) Neurobiology of structure and function, 3, pp. 1-61. , Atwo HL, Sandeman DC, editors. The biology of the crustacean, New York: Academic Press
  • Sandeman, D.C., Sandeman, R.E., Derby, C., Schmidt, M., Morphology of the brain of crayfish, crabs, and spiny lobsters: a common nomenclature for homologous structures (1992) Biol Bull, 183, pp. 304-326
  • Sandeman, D.C., Schoutz, G., Sandeman, R.E., Brain evolution in decapod crustacea (1993) J Exp Zool, 265, pp. 112-133
  • Schramm, M., Dudel, J., Metabotropic glutamate autoreceptors on nerve terminals of crayfish muscle depress or facilitate release (1997) Neurosci Lett, 234, pp. 31-34
  • Shibata, K., Tarui, A., Todoroki, N., Kawamoto, S., Takahashi, S., Kera, Y., Yamada, R., Occurrence of N-methyl-L-aspartate in bivalves and its distribution compared with that of N-methyl-D-aspartate and D,L-aspartate (2001) Comp Biochem Physiol B Biochem Mol Biol, 130, pp. 493-500
  • Si, A., Helliwell, P., Maleszka, R., Effects of NMDA receptor antagonists on olfactory learning and memory in the honeybee (Apis mellifera) (2004) Pharmacol Biochem Behav, 77, pp. 191-197
  • Sinakevitch, I., Farris, S.M., Strausfeld, N.J., Taurine-, aspartate- and glutamate-like immunoreactivity identifies chemically distinct subdivisions of Kenyon cells in the cockroach mushroom body (2001) J Comp Neurol, 439, pp. 352-367
  • Spivak, E.D., The crab Neohelice (=Chasmagnathus) granulata: an emergent animal model from emergent countries (2010) Helgoland Marine Res, 64, pp. 149-154
  • Strausfeld, N.J., Organization of the honey bee mushroom body: representation of the calyx within the vertical and gamma lobes (2002) J Comp Neurol, 450, pp. 4-33
  • Sullivan, J.M., Beltz, B.S., Neural pathways connecting the deutocerebrum and lateral protocerebrum in the brains of decapod crustaceans (2001) J Comp Neurol, 441, pp. 9-22
  • Sweatt, J.D., (2003) Mechanisms of Memory, , London UK: Academic Press
  • Sztarker, J., Strausfeld, N.J., Tomsic, D., Organization of optic lobes that support motion detection in a semiterrestrial crab (2005) J Comp Neurol, 493, pp. 396-411
  • Sztarker, J., Strausfeld, N., Andrew, D., Tomsic, D., Neural organization of first optic neuropils in the littoral crab Hemigrapsus oregonensis and the semiterrestrial species Chasmagnathus granulatus (2009) J Comp Neurol, 513, pp. 129-150
  • Tan, S., Kirk, R.C., Abraham, W.C., McNaughton, N., Effects of the NMDA antagonists CPP and MK-801 on delayed conditional discrimination (1989) Psychopharmacology (Berl), 98, pp. 556-560
  • Todoroki, N., Shibata, K., Yamada, T., Kera, Y., Yamada, R., Determination of N-methyl-D-aspartate in tissues of bivalves by high-performance liquid chromatography (1999) J Chromatogr B Biomed Sci Appl, 728, pp. 41-47
  • Tomsic, D., Berón de Astrada, M., Sztarker, J., Identification of individual neurons reflecting short- and long-term visual memory in an arthropodo (2003) J Neurosci, 23, pp. 8539-8546
  • Troncoso, J., Maldonado, H., Two related forms of memory in the crab Chasmagnathus are differentially affected by NMDA receptor antagonists (2002) Pharmacol Biochem Behav, 72, pp. 251-265
  • Tsien, J.Z., Huerta, P.T., Tonegawa, S., The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory (1996) Cell, 87, pp. 1327-1338
  • Ultsch, A., Schuster, C.M., Laube, B., Betz, H., Schmitt, B., Glutamate receptors of Drosophila melanogaster. Primary structure of a putative NMDA receptor protein expressed in the head of the adult fly (1993) FEBS Lett, 324, pp. 171-177
  • Utting, M., Agricola, H., Sandeman, R., Sandeman, D., Central complex in the brain of crayfish and its possible homology with that of insects (2000) J Comp Neurol, 416, pp. 245-261
  • (2009) Biology of the NMDA receptor, , Van Dongen AM, editor. Boca Raton, FL: CRC Press. Frontiers in Neuroscience
  • Weldon, D.A., Fedorcik, G.G., LoRusso, C.M., Tiburzi, M.J., Lenoci, J.M., Olfactory conditioning impairment following posttraining NMDA receptor blockade in neonatal rats (1997) Neurobiol Learn Mem, 67, pp. 34-42
  • Wu, C.L., Xia, S., Fu, T.F., Wang, H., Chen, Y.H., Leong, D., Chiang, A.S., Tully, T., Specific requirement of NMDA receptors for long-term memory consolidation in Drosophila ellipsoid body (2007) Nat Neurosci, 10, pp. 1578-1586
  • Xia, S., Miyashita, T., Fu, T.F., Lin, W.Y., Wu, C.L., Pyzocha, L., Lin, I.R., Chiang, A.S., NMDA receptors mediate olfactory learning and memory in Drosophila (2005) Curr Biol, 15, pp. 603-615
  • Zannat, M.T., Locatelli, F., Rybak, J., Menzel, R., Leboulle, G., Identification and localization of the NR1 sub-unit homologue of the NMDA glutamate receptor in the honeybee brain (2006) Neurosci Lett, 398, pp. 274-279


---------- APA ----------
Hepp, Y., Tano, M.C., Pedreira, M.E. & Freudenthal, R.A.M. (2013) . NMDA-like receptors in the nervous system of the crab Neohelice granulata: A neuroanatomical description. Journal of Comparative Neurology, 521(10), 2279-2297.
---------- CHICAGO ----------
Hepp, Y., Tano, M.C., Pedreira, M.E., Freudenthal, R.A.M. "NMDA-like receptors in the nervous system of the crab Neohelice granulata: A neuroanatomical description" . Journal of Comparative Neurology 521, no. 10 (2013) : 2279-2297.
---------- MLA ----------
Hepp, Y., Tano, M.C., Pedreira, M.E., Freudenthal, R.A.M. "NMDA-like receptors in the nervous system of the crab Neohelice granulata: A neuroanatomical description" . Journal of Comparative Neurology, vol. 521, no. 10, 2013, pp. 2279-2297.
---------- VANCOUVER ----------
Hepp, Y., Tano, M.C., Pedreira, M.E., Freudenthal, R.A.M. NMDA-like receptors in the nervous system of the crab Neohelice granulata: A neuroanatomical description. J. Comp. Neurol. 2013;521(10):2279-2297.