Activity of respiratory laryngeal motoneurons during fictive coughing and swallowing

Abstract

Membrane potential changes and discharges from 28 laryngeal motoneurons were recorded intracellularly in the caudal nucleus ambiguus of decerebrate, paralyzed and ventilated cats. Electrical activities were recorded from 17 expiratory laryngeal motoneurons (ELMs) with maximal depolarizing membrane potential in early expiration, and from 11 inspiratory laryngeal motoneurons (ILMs) with maximal depolarizing membrane potential in inspiration. Activities during breathing were compared with those observed during fictive coughing and swallowing evoked by electrical stimulation of the superior laryngeal nerves. These non-respiratory behaviors were evidenced in paralyzed animals by characteristic discharge patterns of the phrenic, abdominal nerves and pharyngeal branch of the vagus nerve. We recorded the activity of 11 ELMs and 5 ILMs during coughing in which ELMs, but not ILMs, exhibited increased membrane depolarization and discharge frequencies. Membrane depolarization and discharge frequencies of all ELMs were also significantly increased during swallowing. In addition, membrane depolarization of most ELMs (15/17) was preceded by a short-lasting hyperpolarization due to chloride-dependent inhibitory mechanisms occurring at the onset of swallowing. Out of 10 ILMs tested during swallowing, 7 exhibited membrane depolarization, preceded in 5 cases by a short-lasting hyperpolarization. Discharge frequencies of ILMs were significantly reduced during swallowing. The same pattern of phasic activities of ILMs and ELMs was observed during coughing and breathing, suggesting the involvement of similar excitatory pathways in both behaviors. These results imply that the duration of activation and the discharge frequency of neurons of the central generator for breathing that drive laryngeal motoneurons are enhanced during coughing. During swallowing, in addition to central excitatory mechanisms, laryngeal motoneurons are subjected to an initial inhibition of unknown origin. This inhibition probably contributes to the temporal organization of the swallowing motor sequence.

Microinjection of DLH into the region of the caudal ventral respiratory column in the cat: evidence for an endogenous cough-suppressant mechanism

“…Furthermore, the laryngeal motor pattern during cough can be variable in the same as well as in different experimental preparations (2,16,34,37,43). These observations support the concept that cranial and spinal motor outputs are subject to different regulation specifically during cough (36,43).…”

Multifunctional Laryngeal Premotor Neurons: Their Activities during Breathing, Coughing, Sneezing, and Swallowing

“…ELMs are inhibited at the initiation of swallowing, as shown in (Shiba et al, 1999;Gestreau et al, 2000). The present study showed that BÖ T/preBÖ T EAUG neurons having inhibitory monosynaptic connections with ELMs are suppressed during swallowing.…”

“…In contrast to these behaviors, EAUG neurons were silent during the swallow-related hyperpolarization of ELMs. The swallow-related inhibition preceding excitation in adductor motoneurons (Gestreau et al, 2000) is important for temporal organization of the swallowing motor sequence (Zoungrana et al, 1997). However, the laryngeal motor pattern of swallowing did not use EAUG inhibitory neurons as an inhibitory synaptic source, although the silence of EAUG neurons might indirectly contribute to the swallow-related excitation of ELMs.…”

Neurogenesis of cough, other airway defensive behaviors and breathing: A holarchical system?

“…However, it is known that rhythmic swallow can alternate between repetitive laryngeal coughs (Gestreau et al, 2000). This observation indicates that the system will allow alternating expression of two rhythmic nonbreathing behaviors.…”

“…To be sure, there must be significant temporal correlation between the two behaviors for each to be executed in an appropriate fashion. Indeed, in an example shown in one study (Gestreau et al, 2000) swallows were initiated and completed in the cough expiratory interval. This overlapping expression of two rhythmic behaviors is entirely consistent with the concept that the oscillators for swallow and cough are functionally separate (Jean, 2001;Saito et al, 2003).…”