Skip to main content

Differential Changes of Extracellular Aspartate and Glutamate in the Striatum of Domestic Chicken Evoked by High Potassium or Distress: An In Vivo Microdialysis Study

Neurochemical Research volume 37, pages 1730–1737 (2012)Cite this article

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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. 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

    PubMed  CAS  Google Scholar 

  2. Lovinger D (2010) Neurotransmitter roles in synaptic modulation, plasticity and learning in the dorsal striatum. Neuropharmacology 58:951–961

    PubMed  Article  CAS  Google Scholar 

  3. 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

    PubMed  Article  Google Scholar 

  4. 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

    PubMed  CAS  Google Scholar 

  5. Patterson TA, Rose SPR (1992) Memory in the chick: multiple cues, distinct brain locations. Behav Neurosci 106:465–470

    PubMed  Article  CAS  Google Scholar 

  6. 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

    PubMed  Article  CAS  Google Scholar 

  7. 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

    PubMed  Article  Google Scholar 

  8. 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

    PubMed  Article  CAS  Google Scholar 

  9. Baughman RW, Gilbert CD (1980) Aspartate and glutamate as possible neurotransmitters of cells in layer 6 of the visual cortex. Nature 287:848–850

    PubMed  Article  CAS  Google Scholar 

  10. Wiklund L, Toggenburger G, Cuenod M (1982) Aspartate: possible neurotransmitter in cerebellar climbing fibers. Science 216:78–80

    PubMed  Article  CAS  Google Scholar 

  11. Fagg GE, Foster AC (1983) Amino acid neurotransmitters and their pathways in the mammalian central nervous system. Neuroscience 9:701–719

    PubMed  Article  CAS  Google Scholar 

  12. Yuzaki M, Forrest D, Curran T, Connor JA (1996) Selective activation of calcium permeability by aspartate in Purkinje cells. Science 273:1112–1114

    PubMed  Article  CAS  Google Scholar 

  13. 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

  14. 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

    PubMed  Article  CAS  Google Scholar 

  15. 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

    PubMed  Article  CAS  Google Scholar 

  16. 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

    PubMed  CAS  Google Scholar 

  17. 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

    PubMed  Article  CAS  Google Scholar 

  18. 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

    PubMed  Article  CAS  Google Scholar 

  19. 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

    PubMed  Article  CAS  Google Scholar 

  20. 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

    PubMed  Article  CAS  Google Scholar 

  21. 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

    PubMed  Article  CAS  Google Scholar 

  22. 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

    PubMed  Article  CAS  Google Scholar 

  23. 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

    PubMed  Article  CAS  Google Scholar 

  24. 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

    PubMed  Article  CAS  Google Scholar 

  25. Reubi JC, Toggenburger G, Cuenod M (1980) Asparagine as precursor for transmitter aspartate in corticostriatal fibres. J Neurochem 35:1015–1017

    PubMed  Article  CAS  Google Scholar 

  26. Umeda Y, Sumi T (1989) Evoked release of endogenous amino acids from rat striatal slices and its modulation. Eur J Pharmacol 163:291–297

    PubMed  Article  CAS  Google Scholar 

  27. 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

    PubMed  Article  CAS  Google Scholar 

  28. 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

    PubMed  Article  CAS  Google Scholar 

  29. 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

    PubMed  Article  CAS  Google Scholar 

  30. 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

    PubMed  Article  CAS  Google Scholar 

  31. 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

    PubMed  Article  CAS  Google Scholar 

  32. Csillag A (1999) Striato-telencephalic and striato-tegmental circuits: relevance to learning in domestic chicks. Behav Brain Res 98:227–236

    PubMed  Article  CAS  Google Scholar 

  33. 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

    PubMed  Article  CAS  Google Scholar 

  34. 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

    PubMed  Article  CAS  Google Scholar 

  35. 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

    PubMed  Article  CAS  Google Scholar 

  36. Bálint E, Csillag A (2007) Nucleus accumbens subregions: hodological and immunohistochemical study in the domestic chick (Gallus domesticus). Cell Tissue Res 327:221–230

    PubMed  Article  Google Scholar 

  37. 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

    PubMed  Article  Google Scholar 

  38. 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

    PubMed  Article  CAS  Google Scholar 

  39. 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

    PubMed  Article  CAS  Google Scholar 

  40. 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

    PubMed  Article  Google Scholar 

  41. 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

    PubMed  Article  Google Scholar 

  42. 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

    Article  CAS  Google Scholar 

  43. Timmerman W, Westerink DHC (1997) Brain microdialysis of GABAand glutamate: what does it signify? Synapse 27:242–261

    PubMed  Article  CAS  Google Scholar 

  44. 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

    PubMed  CAS  Google Scholar 

  45. 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

    PubMed  Article  CAS  Google Scholar 

  46. 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

    PubMed  Article  Google Scholar 

  47. 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

    PubMed  Article  CAS  Google Scholar 

  48. 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

    PubMed  Article  CAS  Google Scholar 

  49. Bradford SE, Nadler JV (2004) Aspartate release from rat hippocampal synaptosomes. Neuroscience 128:751–765

    PubMed  Article  CAS  Google Scholar 

  50. 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

    PubMed  Article  CAS  Google Scholar 

  51. 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

    PubMed  Article  CAS  Google Scholar 

  52. 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

    PubMed  Article  CAS  Google Scholar 

  53. Nadler JV (2011) Aspartate release and signalling in the hippocampus. Neurochem Res 36:668–676

    PubMed  Article  CAS  Google Scholar 

Download references

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

Affiliations

  1. Department of Anatomy, Histology and Embryology, Semmelweis University, Tűzoltó u. 58, Budapest, 1094, Hungary

    Gergely Zachar, Eszter Bálint & András Csillag

  2. Department of Pharmacodynamics, Semmelweis University, Nagyvárad Tér 4, Budapest, 1089, Hungary

    Zsolt Wagner, Tamás Tábi & Éva Szökő

Authors
  1. Gergely Zachar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zsolt Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tamás Tábi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Eszter Bálint
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Éva Szökő
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. András Csillag
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gergely Zachar.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11064-012-0783-4

Keywords

  • l-aspartic acid
  • Excitatory neurotransmitters
  • Amino acid
  • Avian
  • Basal ganglia