Global ocean acidification, driven by rising atmospheric CO2, is threatening marine ecosystems and biodiversity, with increasing evidence of its disruptive effects on fish neurobiology and behaviour, yet the mechanisms underpinning its impact on fish neurobiology remain unresolved. Here, we reveal how chronic exposure to future-predicted CO2 levels disrupts brain function in the marine teleost Solea senegalensis, a species with functionally distinct olfactory organs. Using an integrative approach combining electrophysiology, immunohistochemistry, and transcriptomics, we demonstrate that elevated CO2 conditions induce a complex multifaceted disruption in brain physiology. Notably, our findings conflict with the widely held GABAA receptor reversal hypothesis; we observed increased Cl- and CO2 in cerebrospinal fluid and suppressed neural excitability, rather than the predicted loss of Cl- and heightened excitatory signalling. Immunohistochemistry further revealed reduced expression of glial fibrillary acidic protein across multiple brain regions, suggesting glial impairment. Furthermore, transcriptomic profiling of the olfactory bulb uncovered immune modulation, downregulation of neural excitability genes, and upregulation of neuroplasticity, ciliary, and anti-inflammatory pathways, hallmarks of cellular stress adaptation. Notably, genes involved in circadian regulation and thyroid signalling were also dysregulated, pointing to broader neuroendocrine disruption. These findings challenge current relatively simple models of ocean acidification impact and unveil a complex cascade of central and peripheral alterations, including enhanced GABAergic inhibition, immune shifts, glial dysfunction, and disrupted timekeeping mechanisms, likely contributing to the behavioural impairments observed under high CO₂. Challenging current models, our work highlights the need for integrative neurophysiological frameworks to predict marine fish resilience and vulnerability in a changing ocean.
Costa R. A., Olvera A., Sylantyev S., Hubbard P., Manchado M., Power D. M. & Velez Z., 2025. Multifactorial neural disruption in the brain of the Senegalese Sole (Solea senegalensis) under ocean acidification. SSRN. Article.
