D-aspartate (D-Asp) modulates adult neural plasticity and embryonic brain development by promoting cell proliferation, survival and differentiation. Here, developmental changes of the excitatory amino acids (EAAs) L-Glu, L-Asp and D-Asp were determined during the frst postembryonic days, a time window for early learning, in selected brain regions of domestic chickens after chiral separation and capillary electrophoresis. Extracellular concentration (ECC) of EAAs was measured in microdialysis samples from freely moving chicks. ECC of D-Asp (but not L-EAAs) decreased during the frst week of age, with no considerable regional or learning-related variation. ECC of L-Asp and L-Glu (but not of D-Asp) were elevated in the mSt/Ac in response to a rewarding stimulus, suggesting importance of Asp-Glu co-release in synaptic plasticity of basal ganglia. Potassium-evoked release of D-Asp, with a protracted transient, was also demonstrated. D-Asp constitutes greater percentage of total aspartate in the extracellular space than in whole tissue extracts, thus the bulk of D-Asp detected in tissue appears in the extracellular space. Conversely, only a fraction of tissue L-EAAs can be detected in extracellular space. The lack of changes in tissue D-Asp following avoidance learning indicates a tonic, rather than phasic, mechanism in the neuromodulatory action of this amino acid.
Ádám, A. S., 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.
Balázs, D., Csillag, A., Gerber, G. (2012) L-aspartate effects on single neurons and interactions with glutamate in striatal slice preparation from chicken brain. Brain Res. 1474, 1–7.
Bálint, E., Csillag, A. (2007) Nucleus accumbens subregions: hodological and immunohistochemical study in the domestic chick (Gallus domesticus). Cell Tissue Res. 327, 221–230.
Bateson, P. (1966) The characteristics and context of imprinting. Biol. Rev. 41, 177–220.
Csillag, A. (1999) Striato-telencephalic and striato-tegmental circuits: relevance to learning in domestic chicks. Behav. Brain Res. 98, 227–236.
Daisley, J. N., Gruss, M., Rose, S. P. R., 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.
D’Aniello, A. (2007) D-Aspartic acid: an endogenous amino acid with an important neuroendocrine role. Brain Res. Rev. 53, 215–234.
D’Aniello, A., Guiditta, A. (1977) Identifcation of D-aspartic acid in the brain of Octopus vulgaris Lam. J. Neurochem. 29, 1053–1057.
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.
Dermon, C. R., Zikopoulos, B., Panagis, L., Harrison, E., Lancashire, C. L., Mileusnic, R., Stewart, M. G. (2002) Passive avoidance training enhances cell proliferation in 1-day-old chicks. Eur. J. Neurosci. 16, 1267–1274.
Dunlop, D. S., Neidle, A., McHale, D., Dunlop, D. M., Lajtha, A. (1986) The presence of free D-aspartic acid in rodents and man. Biochem. Biophys. Res. Commun. 141, 27–32.
Errico, F., Rossi, S., Napolitano, F., Catuogno, V., Topo, E., Fisone, G., D’Aniello, A., Centonze, D., Usiello, A. (2008) D-aspartate prevents corticostriatal long-term depression and attenuates schizophrenia-like symptoms induced by amphetamine and MK-801. J. Neurosci. 28, 10404–10414.
Errico, F. et al. (2014) Free D-aspartate regulates neuronal dendritic morphology, synaptic plasticity, gray matter volume and brain activity in mammals. Transl. Psychiatry 4, e417.
Fagg, G. E., Matus, A. (1984) Selective association of N-methyl aspartate and quisqualate types of L-glutamate receptor with brain postsynaptic densities. Proc. Natl. Acad. Sci. USA 81, 6876–6880.
Fujii, N. (2005) D-amino acid in elderly tissues. Biol. Pharm. Bull. 28, 1585–1589.
Gibbs, M., Johnston, A. N. B., Mileusnic, R., Crowe, S. F. (2008) A comparison of protocols for passive and discriminative avoidance learning tasks in the domestic chick. Brain Res. Bull. 76, 198–207.
Gundersen, V., Storm-Mathisen, J. (2000) Chapter II Aspartate-neurochemical evidence for a transmitter role. In: Ottersen, O. P., Storm-Mathisen, J. (eds), Handbook of Chemical Neuroanatomy, vol. 18. Amsterdam, Elsevier. pp. 45–62.
Hanics, J., Bálint, E., Milanovich, D., Zachar, G., Adám, A., Csillag, A. (2012) Amygdalofugal axon terminals immunoreactive for L-aspartate or L-glutamate in the nucleus accumbens of rats and domestic chickens: a comparative electron microscopic immunocytochemical study combined with anterograde pathway tracing. Cell Tissue Res. 350, 409–423.
Hanics, J., Teleki, G., Alpár, A., Székely, A. D., Csillag, A. (2016) Multiple amygdaloid divisions of arcopallium send convergent projections to the nucleus accumbens and neighboring subpallial amygdala regions in the domestic chicken: a selective pathway tracing and reconstruction study. Brain Struct. Funct. 222, 301–315.
Hashimoto, A., Kumashiro, S., Nishikawa, T., Oka, T., Takahashi, K., Mito, T., Takashima, S., Doi, N., Mizutani, Y., Yamazaki, T., Kaneko, T., Ootomo, E. (1993) Embryonic development and postnatal changes in free D-aspartate and D-serine in the human prefrontal cortex. J. Neurochem. 61, 348–351.
Hashimoto, A., Oka, T., Nishikawa, T. (1995) Anatomical distribution and postnatal changes in endogenous free D-Aspartate and D-Serine in rat-brain and periphery. Eur. J. Neurosci. 7, 1657–1663.
Horn, G. (2004) Pathways of the past: the imprint of memory. Nat. Rev. Neurosci. 5, 108–120.
Ito, T., Hayashida, M., Kobayashi, S., Muto, N., Hayashi, A., Yoshimura, T., Mori, H. (2016) Serine racemase is involved in D-aspartate biosynthesis. J. Biochem. 160, 345–353.
Matsushima, T., Izawa, E.-I., Yanagihara, S. (2001) D1-receptor dependent synaptic potentiation in the basal ganglia of quail chick. NeuroReport 12, 2831–2837.
McCabe, B. J. (2013) Imprinting. Interdiscip. Rev. Cogn. Sci. 4, 375–390.
Mezey, S., Krivokuca, D., Balint, E., Adorjan, 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.
Miller J. A. (1950) Do tumor proteins contain D-amino acids? A review of the controversy. Cancer Res. 10, 65–72.
Nadler, J. V., Vaca, K. W., White, W. F., Lynch, G. S., Cotman, C. W. (1976) Aspartate and glutamate as possible transmitters of excitatory hippocampal afferents. Nature 260, 538–540.
Nakamori, T., Maekawa, F., Sato, K., Tanaka, K., Ohki-Hamazaki, H. (2013) Neural basis of imprinting behavior in chicks. Dev. Growth Differ. 55, 198–206.
Neidle, A., Dunlop, D. S. (1990) Developmental changes in free D-aspartic acid in the chicken embryo and in the neonatal rat. Life Sci. 46, 1517–1522.
Nuzzo, T. et al. (2017) Decreased free D-aspartate levels are linked to enhanced D-aspartate oxidase activity in the dorsolateral prefrontal cortex of schizophrenia patients. npj Schizophrenia 3, 16.
Puelles, L. (2007) The chick brain in stereotaxic coordinates. Academic Press, San Diego.
Punzo, D., Errico, F., Cristino, L., Sacchi, S., Keller, S., Belardo, C., Luongo, L., Nuzzo, T., Imperatore, R., Florio, E., De Novellis, V., Affnito, O., Migliarini, S., Maddaloni, G., Sisalli, M. J., Pasqualetti, M., Pollegioni, L., Maione, S., Chiariotti, L., Usiello, A. (2016) Age-related changes in D-Aspartate oxidase promoter methylation control extracellular D-Aspartate levels and prevent precocious cell death during brain aging. J. Neurosci. 36, 3064–3078.
Radzishevsky, I., Sason, H., Wolosker, H. (2013) D-serine: physiology and pathology. Curr. Opin. Clin. Nutr. Metab. Care. 16, 72–75.
Reiner, A. (2004) Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473, 377–414.
Rose, S. P. (2000) God’s organism? The chick as a model system for memory studies. Learn. Mem. 7, 1–17.
Schell, M. J., Cooper, O. B., Snyder, S. H. (1997) D-aspartate localizations imply neuronal and neuroendocrine roles. Proc. Natl. Acad. Sci. USA 94, 2013–2018.
Stewart, M. G., Rusakov, D. A. (1995) Morphological changes associated with stages of memory formation in the chick following passive avoidance training. Behav. Brain Res. 66, 21–28.
Topo, E., Soricelli, A., Di Maio, A., D’Aniello, E., Di Fiore, M. M., D’Aniello, A. (2010) Evidence for the involvement of D-aspartic acid in learning and memory of rat. Amino acids 38, 1561–1569.
Venero, C., Sandi, C. (1997) Effects of NMDA and AMPA receptor antagonists on corticosterone facilitation of long-term memory in the chick. Eur. J. Neurosci. 9, 1923–1928.
Wagner, Z., Tabi, T., Zachar, G., Csillag, A., Szoko, E. (2011) Comparison of quantitative performance of three fuorescence labels in CE/LIF analysis of aspartate and glutamate in brain microdi-alysate. Electrophoresis 32, 2816–2822.
Wagner, Z., Tabi, T., Jako, T., Zachar, G., Csillag, A., Szoko, E. (2012) Chiral separation and determination of excitatory amino acids in brain samples by CE-LIF using dual cyclodextrin system. Anal. Bioanal. Chem. 404, 2363–2368.
Wolosker, H., D’Aniello, A., Snyder, S. H. (2000) D-aspartate disposition in neuronal and endocrine tissues: ontogeny, biosynthesis and release. Neuroscience 100, 183–189.
Yamanaka, M., Miyoshi, Y., Ohide, H., Hamase, K., Konno, R. (2012) D-Amino acids in the brain and mutant rodents lacking D-amino-acid oxidase activity. Amino Acids 43, 1811–1821.
Zachar, G., Wagner, Z., Tabi, T., Balint, E., Szoko, E., Csillag, A. (2012) 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.
Zachar, G., Tóth, A. S., Balogh, M., Csillag, A. (2017) Effect of nucleus accumbens lesions on socially motivated behaviour of young domestic chicks. Eur. J. Neurosci. 45, 1606–1612.
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Zachar, G., Jakó, T., Vincze, I. et al. Age-Related and Function-Dependent Regional Alterations of Free L- and D-Aspartate in Postembryonic Chick Brain. BIOLOGIA FUTURA 69, 1–15 (2018). https://doi.org/10.1556/018.68.2018.1.1
- D-aspartic acid
- avian brain
- postembryonic development