Organization of the gymnotiform fish pallium in relation to learning and memory: IV. Expression of conserved transcription factors and implications for the evolution of dorsal telencephalon

J Comp Neurol. 2012 Oct 15;520(15):3395-413. doi: 10.1002/cne.23107.

Abstract

We have cloned the apteronotid homologs of FoxP2, Otx1, and FoxO3. There was, in the case of all three genes, good similarity between the apteronotid and human amino acid sequences: FoxP2, 78%; Otx1, 54%; FoxO3, 71%. The functional domains of these genes were conserved to a far greater extent, on average: FoxP2, 89%; Otx1, 76%; FoxO3, 82%. This led us to hypothesize that the cellular functions of these genes might also be conserved. We used in situ hybridization to examine the distribution of the mRNA transcripts of these genes in the apteronotid telencephalon. We confined our analysis to the pallial regions previously associated with learning about social signals, whose circuitry has been closely examined in the other articles of this series. We found that AptFoxP2 and AptOtx1 transcripts were expressed predominantly in the dorsocentral division of the pallium (DC); the dorsolateral division of the pallium (DL) contained only weakly labeled neurons. In both cases, the distribution of labeled neurons was very heterogeneous, and unlabeled neurons could be found adjacent to strongly labeled ones. In contrast, we found that most neurons in DL strongly expressed AptFoxO3 mRNA, although there was only weak expression in a small number of cells within DC. We briefly discuss the relevance of our results regarding the functional roles of AptFoxP2/AptOtx1-expressing neurons in DC for communication vs. foraging behavior. We extensively discuss the implications of our results for possible homologies between DL and DC and medial and dorsal pallium of tetrapods, respectively.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antisense Elements (Genetics) / genetics
  • Behavior, Animal / physiology
  • Conserved Sequence / genetics
  • Evolution, Molecular
  • Female
  • Forkhead Box Protein O3
  • Forkhead Transcription Factors / genetics
  • Gymnotiformes / anatomy & histology*
  • Gymnotiformes / genetics*
  • Learning / physiology*
  • Male
  • Memory / physiology*
  • Neurons / cytology
  • Neurons / metabolism
  • Otx Transcription Factors / genetics
  • Phylogeny
  • RNA, Messenger / metabolism
  • Sequence Homology, Amino Acid
  • Telencephalon / anatomy & histology*
  • Telencephalon / physiology
  • Transcription Factors / genetics*
  • Xenopus Proteins / genetics
  • Zebrafish Proteins / genetics

Substances

  • Antisense Elements (Genetics)
  • Forkhead Box Protein O3
  • Forkhead Transcription Factors
  • FoxO3 protein, Xenopus
  • FoxP2 protein, zebrafish
  • Otx Transcription Factors
  • RNA, Messenger
  • Transcription Factors
  • Xenopus Proteins
  • Zebrafish Proteins
  • otx1 protein, zebrafish