Acute sleep deprivation (ASD) and cardioprotection: Impact of ASD on oxytocin-mediated sympathetic nervous activation preceding myocardial infarction

• Published in: Neuropeptides (Edinburgh) Vol. 107; p. 102453
• Main Authors: Aghajani, Marjan, Aghajani, Mozhgan, Moghaddam, Ehsan Kazemi, Faghihi, Mahdieh, Imani, Alireza
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier Ltd 01.10.2024
• Subjects: Animals; Cardiac remodeling; Ischemia/reperfusion injury; Male; Myocardial Infarction - metabolism; Neurons - metabolism; Oxytocin; Oxytocin - metabolism; Paraventricular Hypothalamic Nucleus - metabolism; Paraventricular nucleus; Rats; Sleep deprivation; Sleep Deprivation - complications; Sleep Deprivation - metabolism; Sympathetic nervous system; Sympathetic Nervous System - metabolism; Ventricular Remodeling; Ischemia/reperfusion injury; Paraventricular nucleus; Cardiac remodeling; Oxytocin; Sympathetic nervous system; Sleep deprivation
• ISSN: 0143-4179; 1532-2785; 1532-2785
• DOI: 10.1016/j.npep.2024.102453

This study explored how acute sleep deprivation (ASD) before myocardial ischemia influences oxytocin release from paraventricular (PVN) neurons and its correlation with sympathetic nervous system (SNS) activity post-acute sleep loss, impacting subsequent left ventricular (LV) remodeling following myocardial infarction (MI). The study was conducted in two phases: induction of ASD, inducing MI, blood sampling, euthanizing animals and collecting their heart and brain for histological and gene expression evaluations. The animals in first and second phase were euthanized 24 h and 14 days after MI, respectively. Pre-MI ASD, accompanied by increased serum epinephrine levels within 24 h of MI, upregulated oxytocin and cFos expression in the PVN. Also, pre-MI ASD resulted in decreased serum PAB levels 14 days post-MI (P < 0.001). While notable echocardiographic changes were seen in MI versus sham groups, ASD demonstrated protective effects. This was evidenced by reduced infarct size, elevated TIMP1, MMP2, and MMP9 in the LV of SD + MI animals versus MI alone (P < 0.05). Additionally, histological analysis showed reduced LV fibrosis in pre-MI ASD subjects (P < 0.05). Our study supports the notion that activation of oxytocin neurons within the PVN subsequent to ASD interacts with autonomic centers in the central nervous system. This enhanced sympathetic outflow to the heart prior to MI triggers a preconditioning response, thereby mediating cardioprotection through decreased oxidative stress biomarkers and regulated extracellular matrix (ECM) turnover. •ASD prevents adverse cardiac remodeling after MI.•Short-term sympathetic activation by ASD leads to adaptive cardiac remodeling.•Oxytocinergic neuron activation plays a protective role.•Balanced sympathetic activity challenges the view of sustained sympathetic overdrive being harmful.