Inhalation of a pulmonary irritant modulates activity of lumbosacral spinal neurons receiving colonic input in rats

Abstract

The purpose of the present study was to determine whether an intraspinal nociceptive pathway from the lungs modulated activity of spinal neurons that also received afferent input from the colon. Extracellular potentials of single lumbosacral (L6–S2) spinal neurons were recorded in pentobarbital-anesthetized, paralyzed, and ventilated male rats. The lower airways and lungs were irritated by injecting ammonia vapor over a 30% NH4OH solution into the inspiratory line of the ventilator (0.5 ml, 20 s). Graded colorectal distension (CRD; 20–60 mmHg, 20 s) was produced by air inflation of a balloon. Inhaled ammonia (IA) altered activity of 31/51 (61%) lumbosacral spinal neurons responding to noxious CRD (60 mmHg, 20 s). In contrast, IA changed activity of 3/30 (10%) spinal neurons with somatic fields that did not respond to colorectal inputs. IA decreased activity of 16/31 (52%) spinal neurons and increased activity of the other 15 neurons with colorectal input. Multiple patterns of viscerovisceral convergent spinal neurons with excitatory and inhibitory responses to CRD and IA were observed; 87% (27/31) of the viscerovisceral convergent neurons also responded to innocuous and/or noxious stimuli of somatic fields. Bilateral cervical vagotomy abolished responses to IA in 2/8 tested neurons, indicating that the remaining 6 neurons had input originating from sympathetic afferent fibers. Rostral C1 spinal transection did not abolish inhibitory responses to IA in 4/4 neurons, but L2 transection eliminated inhibitory responses to IA in 3/3 neurons. These results indicated that irritation of the lower airways modulated activity of lumbosacral spinal neurons with colorectal input. It might contribute to intraspinal cross talk between the colon and lungs.