Elsevier

Neuroscience

Volume 133, Issue 3, 2005, Pages 625-633
Neuroscience

Behavioural neuroscience
Early socio-emotional experience induces expression of the immediate-early gene Arc/arg3.1 (activity-regulated cytoskeleton-associated protein/activity-regulated gene) in learning-relevant brain regions of the newborn chick

https://doi.org/10.1016/j.neuroscience.2005.02.048Get rights and content

Abstract

We have cloned a full-length complementary DNA from the chicken (Gallus gallus domesticus), which encodes a polypeptide that exhibits ∼75% identity to the product of the mammalian gene Arc (activity-regulated cytoskeleton-associated protein), also known as arg3.1 (activity-regulated gene). Since this gene is an immediate-early gene that has been suggested to play a role in synaptic plasticity and learning and memory processes, its expression has been analyzed in a juvenile form of learning, namely, filial imprinting. Our results demonstrate that Arc/arg3.1 mRNA is detectable in the newborn chick brain, and that at this early age the level of this transcript can be altered by brief sensory/emotional experience. After postnatal exposure to a novel 30-min auditory imprinting stimulus, Arc/arg3.1 mRNA was found to be significantly increased in two higher associative areas, the mesopallium intermediomediale (P=0.002) and the nidopallium dorso-caudale (P=0.031), compared with naïve controls. The transcript level was also significantly elevated after imprinting in Area L pallii (P=0.045), which is analogous to the mammalian auditory cortex. In addition, increases were seen in the medio-rostral nidopallium/mesopallium (P=0.054), which is presumed to be the analog of the mammalian prefrontal cortex, and the hyperpallium intercalatum (P=0.054), but these did not quite reach significance. We discuss these data in the light of those obtained in an earlier study, in the same paradigm, for the avian immediate-early gene, zenk (an acronym for zif-268, egr-1, ngfi-a and krox-24, which are different names for the orthologous mammalian gene).

We conclude that, although both the Arc/arg3.1 and zenk genes are induced by auditory imprinting, they are significantly up-regulated in different learning-relevant brain regions. It is, therefore, evident that they must be activated by different mechanisms.

Section snippets

RNA isolation and cDNA synthesis

Total RNA was isolated from the brains of 1-day-old chicks (Gallus gallus domesticus) and adult rats (Rattus norvegicus) and treated with RNase-free DNase I (Promega, Mannheim, Germany). First-strand cDNA was then synthesized using either random nonamers (Stratagene, Amsterdam Zuidoost, The Netherlands) or the primer RoRidT17 (5′-ATCGATGGTCGACGCATGCGGATCCAAAGCTTGAATTCGAGCTCT17-3′; Harvey et al., 1991) and Moloney murine leukemia virus reverse transcriptase (Promega).

Amplification of a rat Arc/arg3.1 partial cDNA

An ∼1.2 kb cDNA fragment was

Results

By screening a chicken brain library with a rat Arc/arg3.1 cDNA probe, and the subsequent application of a nested RACE protocol (Frohman and Martin 1989, Harvey et al 1991, Stühmer et al 1996), we have isolated a full-length cDNA that encodes a polypeptide of 404 amino acids (Fig. 1), with a predicted molecular weight of 46,307 Da. This polypeptide exhibits 74%, 74% and 75% identity to the mouse (EMBL accession number AF162777), rat (Link et al., 1995; EMBL accession number Z46925) and human (

Discussion

We describe here the isolation of a full-length cDNA that encodes a 404 amino-acid protein that displays ∼75% sequence identity to mammalian Arc/arg3.1 proteins, defining it as the chicken orthologue. The sequence of this clone has been used to design a specific 45-base oligonucleotide, which has been used in in situ hybridization experiments to investigate changes in the expression of the Arc/arg3.1 gene in response to a short (30-min) acoustic imprinting paradigm in newborn chicks. This

Acknowledgments

This work was supported in part by the Deutsche Forschungsgemeinschaft (SFB444/A5 to M.G.D.), an award from the Fonds der Chemischen Industrie (to M.G.D.), and the VolkswagenStiftung (to K.B.). We thank Agata Blaszcyk-Wewer and Sönke Harder (Hamburg) for DNA sequencing and oligonucleotide synthesis, respectively.

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