Myocardial infarction reduces cardiac nociceptive neurotransmission through the vagal ganglia
Siamak Salavatian, Jonathan D. Hoang, Naoko Yamaguchi, Zulfiqar Ali Lokhandwala, Mohammed Amer Swid, John Andrew Armour, Jeffrey L. Ardell, Marmar Vaseghi
Siamak Salavatian, Jonathan D. Hoang, Naoko Yamaguchi, Zulfiqar Ali Lokhandwala, Mohammed Amer Swid, John Andrew Armour, Jeffrey L. Ardell, Marmar Vaseghi
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Research Article Cardiology Neuroscience

Myocardial infarction reduces cardiac nociceptive neurotransmission through the vagal ganglia

Abstract

Myocardial infarction causes pathological changes in the autonomic nervous system, which exacerbate heart failure and predispose to fatal ventricular arrhythmias and sudden death. These changes are characterized by sympathetic activation and parasympathetic dysfunction (reduced vagal tone). Reasons for the central vagal withdrawal and, specifically, whether myocardial infarction causes changes in cardiac vagal afferent neurotransmission that then affect efferent tone, remain unknown. The objective of this study was to evaluate whether myocardial infarction causes changes in vagal neuronal afferent signaling. Using in vivo neural recordings from the inferior vagal (nodose) ganglia and immunohistochemical analyses, structural and functional alterations in vagal sensory neurons were characterized in a chronic porcine infarct model and compared with normal animals. Myocardial infarction caused an increase in the number of nociceptive neurons but a paradoxical decrease in functional nociceptive signaling. No changes in mechanosensitive neurons were observed. Notably, nociceptive neurons demonstrated an increase in GABAergic expression. Given that nociceptive signaling through the vagal ganglia increases efferent vagal tone, the results of this study suggest that a decrease in functional nociception, possibly due to an increase in expression of inhibitory neurotransmitters, may contribute to vagal withdrawal after myocardial infarction.

Authors

Siamak Salavatian, Jonathan D. Hoang, Naoko Yamaguchi, Zulfiqar Ali Lokhandwala, Mohammed Amer Swid, John Andrew Armour, Jeffrey L. Ardell, Marmar Vaseghi

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Figure 5

Nodose neural responses to specific cardiac interventions.

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Nodose neural responses to specific cardiac interventions. (A) Percentag...
(A) Percentages of neurons with significant changes in absolute firing rates in response to ventricular pacing (VP), aortic occlusion (AO), epicardial mechanical stimulation (EMS), inferior vena cava (IVC) occlusion, and nociceptive stimuli (NS) are shown. (B) Percentage of chemosensitive neurons that responded to each specific chemical stimulus is shown (capsaicin, CAPS; bradykinin, BRADY; veratridine, VERAT) in normal and MI animals. (C) Percentage of neurons that were excited or inhibited in response to each cardiac stressor is shown. The predominant response to nociceptive stimuli in normal animals was excitatory (an increase in firing rate: +) while the predominant response to nociceptive chemicals in RCA-infarcted animals was inhibitory (a decrease in firing rate: -). (D) The percentage of neurons that were excited or inhibited for each specific chemical in normal and RCA-infarcted animals is shown. Both capsaicin and bradykinin caused statistically significant decreases in firing rates. Fisher’s exact test with Dunn’s correction for multiple comparisons was used to compare the percentage of neurons in normal and MI animals. **0.001 < P ≤ 0.01, #P ≤ 0.001 compared with normal animals.