Characterization of thoracic spinal neurons with noxious convergent inputs from heart and lower airways in rats

Abstract

Respiratory symptoms experienced in some patients with cardiac diseases may be due to convergence of noxious cardiac and pulmonary inputs onto neurons of the central nervous system. For example, convergence of cardiac and respiratory inputs onto single solitary tract neurons may be in part responsible for integration of regulatory and defensive reflex control. However, it is unknown whether inputs from the lungs and heart converge onto single neurons of the spinal cord. The present aim was to characterize upper thoracic spinal neurons responding to both noxious stimuli of the heart and lungs in rats. Extracellular potentials of single thoracic (T3) spinal neurons were recorded in pentobarbital anesthetized, paralyzed, and ventilated male rats. A catheter was placed in the pericardial sac to administer bradykinin (BK, 10 μg/ml, 0.2 ml, 1 min) as a noxious cardiac stimulus. The lung irritant, ammonia, obtained as vapor over a 30% solution of NH 4 OH was injected into the inspiratory line of the ventilator (0.5-1.0 ml over 20 sec). Intrapericardial bradykinin (IB) altered activity of 58/65 (89%) spinal neurons the responded to inhaled ammonia (IA). Among those cardiopulmonary convergent neurons, 81% (47/58) were excited by both IA and IB, and the remainder had complex response patterns. Bilateral cervical vagotomy revealed that vagal afferents modulated but did not eliminate responses of individual spinal neurons to IB and IA. The convergence of pulmonary and cardiac nociceptive signaling in the spinal cord may be relevant to situations where a disease process in one organ influences the behavior of the other.

Sympatho-excitatory response to pulmonary chemosensitive spinal afferent activation in anesthetized, vagotomized rats

“…Consistent with the current study, a study by Qin et al. () showed that noxious stimuli applied to both the lung and the heart altered activity within the same convergent T3 spinal neurons. In the present study, chemical stimulation of the ventral lung visceral pleura evoked similar pressor responses to that of cardiac afferent activation.…”

“…Early studies indicated that tracheal afferent nerve fibers originated in the C1 and T1-T4 DRG (Dalsgaard and Lundberg 1984; Kummer et al 1992) and that pulmonary spinal afferent activity can be recorded from T2 to T4 (Kostreva et al 1981), the same upper thoracic segments in which cardiac sympathetic afferents pass (Wang et al 2014). Consistent with the current study, a study by Qin et al (2007) showed that noxious stimuli applied to both the lung and the heart altered activity within the same convergent T3 spinal neurons. In the present study, chemical stimulation of the ventral lung visceral pleura evoked similar pressor responses to that of cardiac afferent activation.…”

Visceral organ cross-sensitization — An integrated perspective

“…Studies in cat (Ammons and Foreman, 1984), monkey (Ammons et al, 1984) and rat (Qin et al, 2007c) have shown that distension of the gallbladder (Ammons et al, 1984; Ammons and Foreman, 1984) or stomach (Qin et al, 2007c) activates thoracic spinothalamic tract neurons responsive to noxious chemical stimulation of the heart. Likewise, airway irritants (e.g., ammonia, cigarette smoke) have been shown to excite rat thoracic spinal neurons that also respond to esophageal distension (Hummel et al, 1997) or intrapericardial administration of bradykinin (Euchner-Wamser et al, 1994; Qin et al, 2007d). …”

Silent Myocardial Ischemia

“…Cardiac afferents project to the same spinothalamic tract neurons as esophageal, lung, gastric, and gall bladder afferents. [52][53][54][55] This might contribute to the well known clinical difficulty in localizing visceral pain, and could mask the diagnosis of myocardial ischemia in some patients. Finally, afferents from other organs might modulate cardiac pain perception.…”