Abstract
It has long been proposed that l-aspartate (Asp) is an excitatory neurotransmitter similar to l-glutamate (Glu) but with distinct signaling properties. The presence of Asp in excitatory synapses of the medial striatum/nucleus accumbens of domestic chicks suggests that Asp plays a role of neurotransmitter also in the avian brain. Neurotransmitters are released from the presynaptic bouton mostly by Ca2+ dependent exocytosis. We used in vivo microdialysis to monitor the simultaneous changes of the extracellular levels of Asp and Glu in the medial striatum of young post-hatch domestic chicks. Microdialysis samples were collected from freely moving birds at 5 min intervals and analysed off-line using capillary electrophoresis. Event-related elevations of extracellular Glu and Asp concentrations in response to handling stress and to high KCl (50 mM) were observed. Increase of Glu and Asp on handling stress was 200 and 250 %, whereas on KCl stimulation the values were 300 and 1,000 %, respectively, if stress was applied before high KCl, and 150 and 200 %, respectively, in the absence of stress. In most cases, the amino acids showed correlated changes, Asp concentrations being consistently smaller at resting but exceeding Glu during stimulation. Using Ca2+ free medium, the KCl triggered elevation of Glu was reduced. When KCl stimulation was combined with tetrodotoxin infusion, there was no significant elevation in Asp or in Glu suggesting that most of the extracellular excitatory amino acids were released by synaptic mechanisms. The results support the suggestion that Asp is co-released with Glu and may play a signaling role (as distinct from that of glutamate) in the striatum of birds.
Similar content being viewed by others
References
Carlsson M, Carlsson A (1990) Interactions between glutamatergic and monoaminergic systems within the basal ganglia—implications for schizophrenia and Parkinson’s disease. TINS 13:272–276
Lovinger D (2010) Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58:951–961
Izawa E-I, Zachar G, Aoki N, Koga K, Matsushima T (2002) Lesions of ventro-medial basal ganglia impair the reinforcement but not recall of memorized color discrimination in domestic chicks. Behav Brain Res 136:405–414
Izawa E, Zachar G, Yanagihara S, Matsushima T (2003) Localized lesion of caudal part of lobus parolfactorius caused impulsive choice in the domestic chick: evolutionarily conserved function of ventral striatum. J Neurosci 23:1894–1902
Patterson TA, Rose SPR (1992) Memory in the chick: multiple cues, distinct brain locations. Behav Neurosci 106:465–470
Gilbert DB, Patterson TA, Rose SPR (1991) Dissociation of brain sites necessary for registration and storage of memory for a one-trial passive avoidance task in the chick. Behav Neurosci 105:553–561
Ádám AS, Csillag A (2006) Differential distribution of l-aspartate- and l-glutamate-immunoreactive structures in the arcopallium and medial striatum of the domestic chick (Gallus domesticus). J Comp Neurol 498:266–276
Nadler JV, Vaca KV, White WF, Lynch GS, Cotman CV (1976) Aspartate and glutamate as possible neurotransmitter of excitatory hippocampal afferents. Nature 260:538–540
Baughman RW, Gilbert CD (1980) Aspartate and glutamate as possible neurotransmitters of cells in layer 6 of the visual cortex. Nature 287:848–850
Wiklund L, Toggenburger G, Cuenod M (1982) Aspartate: possible neurotransmitter in cerebellar climbing fibers. Science 216:78–80
Fagg GE, Foster AC (1983) Amino acid neurotransmitters and their pathways in the mammalian central nervous system. Neuroscience 9:701–719
Yuzaki M, Forrest D, Curran T, Connor JA (1996) Selective activation of calcium permeability by aspartate in Purkinje cells. Science 273:1112–1114
Gundersen V, Storm-Mathisen J (2000) Aspartate—neurochemical evidence for transmitter role. In: Ottersen OP, Storm-Mathisen J (eds) Handbook of chemical neuroanatomy, vol 18. Glutamate. Elsevier, North Holland, pp 45–62
Ottersen OP, Storm-Mathisen J (1985) Different neuronal localization of aspartate-like and glutamate-like immunoreactivities in the hippocampus of the rat, guinea-pig and senegalese baboon (Papio papio) with a note on the distribution of gammaaminobutyrate. Neuroscience 16:589–606
Aoki E, Semba R, Kato K, Kashiwamata S (1987) Purification of specific antibody against aspartate and immunocytochemical localization of aspatergic neurons in the rat brain. Neuroscience 21:755–765
Gundersen V, Chaudhry FA, Bjaalle JG, Fonnum F, Ottersen OP, Storm-Mathisen J (1998) Synaptic vesicular localization and exocytosis of l-aspartate in excitatory nerve terminals: a quantitative immunogold analysis in rat hippocampus. J Neurosci 18:6059–6070
Gundersen V, Holten AT, Storm-Mathisen J (2004) GABAergic synapses in hippocampus exocytose aspartate on to NMDA receptors: quantitative immunogold evidence for co-transmission. Mol Cell Neurosci 26:156–165
Girault JA, Barbeito L, Spampinato U, Gozlan H, Glowinski J, Besson MJ (1986) In vivo release of endogenous amino acids from the rat striatum: further evidence for a role of glutamate and aspartate in corticostriatal neurotransmission. J Neurochem 47:98–106
Nadler JV, Martin D, Bustos GA, Burke SR, Bowe MA (1990) Regulation of glutamate and aspartate release from the Schaffer collaterals and other projections of CA3 hippocampal pyramidal cells. Prog Brain Res 83:115–130
Burke SR, Nadler JV (1988) Regulation of glutamate and aspartate release from slices of the hippocampal CA1 area: effects of adenosine and baclofen. J Neurochem 51:1541–1551
Szerb JC (1988) Changes in the relative amounts of aspartate and glutamate released and retained in hippocampal slices during stimulation. J Neurochem 50:219–224
Zhou M, Peterson CL, Lu YB, Nadler JV (1995) Release of glutamate and aspartate from CA1 synaptosomes: selective modulation of aspartate release by ionotropic glutamate receptor ligands. J Neurochem 64:1556–1566
Flint RS, Rea MA, McBride WJ (1981) In vitro release of endogenous amino acids from granule cell-, stellate cell-, and climbing fiber-deficient cerebella. J Neurochem 37:1425–1430
Maura G, Barzizza A, Folghera S, Raiteri M (1991) Release of endogenous aspartate from rat cerebellum slices and synaptosomes: inhibition mediated by a 5-HT2 receptor and by a 5-HT1 receptor of a possibly novel subtype. Naunyn Schmiedebergs Arch Pharmacol 343:229–236
Reubi JC, Toggenburger G, Cuenod M (1980) Asparagine as precursor for transmitter aspartate in corticostriatal fibres. J Neurochem 35:1015–1017
Umeda Y, Sumi T (1989) Evoked release of endogenous amino acids from rat striatal slices and its modulation. Eur J Pharmacol 163:291–297
Kimura M, Yamanishi Y, Hanada T, Kagaya T, Kuwada M, Watanabe T, Katayama K, Nishizawa Y (1995) Involvement of P-type calcium channels in high potassium elicited release of neurotransmitters from rat brain slices. Neuroscience 66:609–615
Paulsen RE, Fonnum F (1989) Role of glial cells for the basal and Ca2+-dependent K+-evoked release of transmitter amino acids investigated by microdialysis. J Neurochem 52:1823–1829
Lada MW, Vickroy TW, Kennedy RT (1998) Evidence for neuronal origin and metabotropic receptor-mediated regulation of extracellular glutamate and aspartate in rat striatum in vivo following electrical stimulation of the prefrontal cortex. J Neurochem 70:617–625
Daisley JN, Gruss M, Rose SPR, Braun K (1998) Passive avoidance training and recall are associated with increased glutamate levels in the intermediate medial hyperstriatum centrale of the day-old chick. Neural Plast 6:53–61
Gruss M, Braun K (1996) Stimulus-evoked increase of glutamate in the mediorostral neostriatum/hyperstriatum ventrale of domestic chick after auditory filial imprinting: an in vivo microdialysis study. J Neurochem 66:1167–1173
Csillag A (1999) Striato-telencephalic and striato-tegmental circuits: relevance to learning in domestic chicks. Behav Brain Res 98:227–236
Csillag A, Bálint E, Adám A, Zachar G (2008) The organisation of the basal ganglia in the domestic chick (Gallus domesticus): anatomical localisation of DARPP-32 in relation to glutamate. Brain Res Bull 76:183–191
Csillag A, Székely AD, Stewart MG (1997) Synaptic terminals immunolabelled against glutamate in the lobus parolfactorius of domestic chicks (Gallus domesticus) in relation to afferents from the archistriatum. Brain Res 750:171–179
Wagner Z, Tábi T, Zachar G, Csillag A, Szökő E (2011) Comparison of quantitative performance of three fluorescence labels in CE/LIF analysis of aspartate and glutamate in brain microdialysate. Electrophoresis 32:2816–2822
Bálint E, Csillag A (2007) Nucleus accumbens subregions: hodological and immunohistochemical study in the domestic chick (Gallus domesticus). Cell Tissue Res 327:221–230
Bálint E, Mezey S, Csillag A (2011) Efferent connections of nucleus accumbens subdivisions of the domestic chicken (Gallus domesticus): an anterograde pathway tracing study. J Comp Neurol 519:2922–2953
Herrera-Marschitz M, Goiny M, You ZB, Meana JJ, Pettersson E, Rodriguez-Puertas R, Xu ZQ, Terenius L, Hökfelt T, Ungerstedt U (1997) On the release of glutamate and aspartate in the basal ganglia of the rat: interactions with monoamines and neuropeptides. Neurosci Biobehav Rev 21:489–495
Reid MS, Fox L, Ho LB, Berger SP (2000) Nicotine stimulation of extracellular glutamate levels in the nucleus accumbens: neuropharmacological characterization. Synapse 35:129–136
Miguéns M, Del Olmo N, Higuera-Matas A, Torres I, García-Lecumberri C, Ambrosio E (2008) Glutamate and aspartate levels in the nucleus accumbens during cocaine self-administration and extinction: a time course microdialysis study. Psychopharmacology 196:303–313
Vallée N, Rostain JC, Boussuges A, Risso JJ (2009) Comparison of nitrogen narcosis and helium pressure effects on striatal amino acids: a microdialysis study in rats. Neurochem Res 34:835–844
Wang M, Slaney T, Mabrouk O, Kennedy RT (2010) Collection of nanoliter microdialysate fractions in plugs for off-line in vivo chemical monitoring with up to 2 s temporal resolution. J Neurosci Meth 190:39–48
Timmerman W, Westerink DHC (1997) Brain microdialysis of GABAand glutamate: what does it signify? Synapse 27:242–261
Patneau DK, Mayer ML (1990) Structure-activity relationships for amino acid transmitter candidates acting at N-methyl-d-aspartate and quisqualate receptors. J Neurosci 10:2385–2399
Brautigan RA, Eagles DA (1998) Activation of NMDA and non-NMDA receptors by l-aspartate in the suprachiasmatic nucleus of the rat. Cell Signal 10:85–90
D’Aniello S, Somorjai I, Garcia-Fernàndez J, Topo E, D’Aniello A (2011) d-Aspartic acid is a novel endogenous neurotransmitter. FASEB J 25:1014–1027
Yatsushiro S, Yamada H, Kozaki S, Kumon H, Michibata H, Yamamoto A, Moriyama Y (1997) L-aspartate but not the D form is secreted through microvesicle-mediated exocytosis and is sequestered through Na+-dependent transporter in rat pinealocytes. J Neurochem 69:340–347
Balcar VJ, Johnston GA (1972) The structural specificity of the high affinity uptake of l-glutamate and l-aspartate by rat brain slices. J Neurochem 19:2657–2666
Bradford SE, Nadler JV (2004) Aspartate release from rat hippocampal synaptosomes. Neuroscience 128:751–765
Kim PM, Duan X, Huang AS, Liu CY, Ming GL, Song H, Snyder SH (2010) Aspartate racemase, generating neuronal d-aspartate, regulates adult neurogenesis. Proc Natl Acad Sci USA 107:3175–3179
Mezey S, Krivokuca D, Bálint E, Adorján A, Zachar G, Csillag A (2012) Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus). J Comp Neurol 520:100–116
Cavallero A, Marte A, Fedele E (2009) l-Aspartate as an amino acid neurotransmitter: mechanisms of the depolarization-induced release from cerebrocortical synaptosomes. J Neurochem 110:924–934
Nadler JV (2011) Aspartate release and signalling in the hippocampus. Neurochem Res 36:668–676
Acknowledgments
This work has been supported by the Hungarian National Scientific Research Fund (OTKA 63415 and 73219) and TÁMOP-4.2.1/B-09/1/KMR-2010-0001.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Zachar, G., Wagner, Z., Tábi, T. et al. Differential Changes of Extracellular Aspartate and Glutamate in the Striatum of Domestic Chicken Evoked by High Potassium or Distress: An In Vivo Microdialysis Study. Neurochem Res 37, 1730–1737 (2012). https://doi.org/10.1007/s11064-012-0783-4
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11064-012-0783-4