Frontiers in Pharmacology (Jun 2020)

Environmental Enrichment Improved Learning and Memory, Increased Telencephalic Cell Proliferation, and Induced Differential Gene Expression in Colossoma macropomum

  • Patrick Douglas Corrêa Pereira,
  • Ediely Pereira Henrique,
  • Danillo Monteiro Porfírio,
  • Caio César de Sousa Crispim,
  • Maitê Thaís Barros Campos,
  • Renata Melo de Oliveira,
  • Isabella Mesquita Sfair Silva,
  • Luma Cristina Ferreira Guerreiro,
  • Tiago Werley Pires da Silva,
  • Anderson de Jesus Falcão da Silva,
  • João Batista da Silva Rosa,
  • Dmitre Leonardo Ferreira de Azevedo,
  • Cecília Gabriella Coutinho Lima,
  • Cintya Castro de Abreu,
  • Carlos Santos Filho,
  • Domingos Luiz Wanderley Picanço Diniz,
  • Nara Gyzely de Morais Magalhães,
  • Cristovam Guerreiro-Diniz,
  • Cristovam Wanderley Picanço Diniz,
  • Daniel Guerreiro Diniz,
  • Daniel Guerreiro Diniz

DOI
https://doi.org/10.3389/fphar.2020.00840
Journal volume & issue
Vol. 11

Abstract

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Fish use spatial cognition based on allocentric cues to navigate, but little is known about how environmental enrichment (EE) affects learning and memory in correlation with hematological changes or gene expression in the fish brain. Here we investigated these questions in Colossoma macropomum (Teleostei). Fish were housed for 192 days in either EE or in an impoverished environment (IE) aquarium. EE contained toys, natural plants, and a 12-h/day water stream for voluntary exercise, whereas IE had no toys, plants, or water stream. A third plus maze aquarium was used for spatial and object recognition tests. Compared with IE, the EE fish showed greater learning rates, body length, and body weight. After behavioral tests, whole brain tissue was taken, stored in RNA-later, and then homogenized for DNA sequencing after conversion of isolated RNA. To compare read mapping and gene expression profiles across libraries for neurotranscriptome differential expression, we mapped back RNA-seq reads to the C. macropomum de novo assembled transcriptome. The results showed significant differential behavior, cell counts and gene expression in EE and IE individuals. As compared with IE, we found a greater number of cells in the telencephalon of individuals maintained in EE but no significant difference in the tectum opticum, suggesting differential plasticity in these areas. A total of 107,669 transcripts were found that ultimately yielded 64 differentially expressed transcripts between IE and EE brains. Another group of adult fish growing in aquaculture conditions were either subjected to exercise using running water flow or maintained sedentary. Flow cytometry analysis of peripheral blood showed a significantly higher density of lymphocytes, and platelets but no significant differences in erythrocytes and granulocytes. Thus, under the influence of contrasting environments, our findings showed differential changes at the behavioral, cellular, and molecular levels. We propose that the differential expression of selected transcripts, number of telencephalic cell counts, learning and memory performance, and selective hematological cell changes may be part of Teleostei adaptive physiological responses triggered by EE visuospatial and somatomotor stimulation. Our findings suggest abundant differential gene expression changes depending on environment and provide a basis for exploring gene regulation mechanisms under EE in C. macropomum.

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