The nucleus retroambigualis controls laryngeal muscle activity during vocalization in the cat

Abstract

The purpose of this study was to determine (1) whether the nucleus retroambigualis (NRA) plays an essential role in periaqueductal gray (PAG)-induced vocalization and (2) which NRA neurons are involved in the projection from the PAG to laryngeal motoneurons. Bilateral injections of the neurotoxin kainic acid into the NRA in decerebrate cats abolished PAG-induced vocalization; PAG stimulation after the injections no longer modulated vocal fold adductor or tensor activity, and only tonically, but no longer phasically, activated the abdominal muscles. In contrast, PAG-induced inspiratory excitation remained even after the injections. These results suggest that the NRA is essential for the vocal activation of the laryngeal adductor and abdominal muscles, and that an additional pathway from the PAG to respiratory motoneurons other than through the NRA is important for mediating PAG-induced inspiratory activation. Secondly, axonal projections of NRA neurons to the contralateral nucleus ambiguus (NA) were studied electrophysiologically. Five expiratory neurons, which had decrementing (n=4) or constant (n=1) firing patterns, were identified as both having axonal projections to the NA and receiving inputs from the PAG. Furthermore, following NA stimulation many constant-latency action potentials of silent cells were recorded in the vicinity of the NRA, where many silent cells were also orthodromically activated by PAG stimulation. No NRA augmenting expiratory neurons could be antidromically activated from the NA. It is suggested that the NRA and adjacent reticular formation integrate inputs from the PAG and send outputs to laryngeal motoneurons for vocalization.

The Midbrain Periaqueductal Gray Control of Respiration

“…The elimination of the PAG control of respiratory neuronal circuitry may contribute to the animal's inability to physically express emotions. Our results also support previous observations on the role of PAG in correlating respiratory and intralaryngeal activity not only in cats (Magoun et al, 1937;Bandler and Carrive, 1988;Davis et al, 1993;Zhang et al, 1994;Shiba et al, 1997) but also in monkey (Jürgens and Pratt, 1979;Larson, 1985;Larson and Kistler, 1986) and humans (Mead and Reid, 1988;Holstege and Ehling, 1994). Our results demonstrate that the PAG has a similar control over respiration as over micturition, mating behavior, cardiovascular systems, nociception, and other levelsetting systems (Fig.…”

“…The present results show that the PAG induces an expiratory drive by recruiting the internal intercostal and internal and external abdominal oblique muscles before a mew. According to Shiba et al (1997) in the cat, expiration-related neurons and other "silent" cells in the nucleus retroambiguus as well as neurons in the reticular formation medially adjoining the NRA are activated by the PAG and could play an important role in shaping the vocal expiratory outflow. The large increases in the tracheal pressure (up to 40 cm H 2 O) demonstrate that the PAG integrates the expiratory and laryngeal activity required for the generation of vocalization.…”

Multifunctional Laryngeal Motoneurons: an Intracellular Study in the Cat

“…Hostege (1989) proposed the final common pathway for vocalization: the projection from the PAG via the nucleus retroambigualis (NRA) to laryngeal motoneurons. Our previous study showed that neurons in the vicinity of the NRA are part of the neuronal network providing vocal-related drives to ELMs but do not participate in producing respiratory-related ELM activity (Shiba et al, 1997). Furthermore, decrementing patterns of membrane potential trajectories of EL Ms during the expiratory phase in eupnea changed to bell-shaped patterns during vocalization.…”

“…We suggest that vocalization-related abductor activity balances vocal fold adduction during vocalization and prevents excessive narrowing of the glottis. The PAG-NRA projection is not important for PAG-induced abductor activation (Shiba et al, 1997). However, PAG neurons also project, through the PCS, to the region between the Bötzinger complex and rostral ventral respiratory group (BÖ T/rVRG) (Sakamoto et al, 1996b), which is a key area for respiratory rhythmogenesis (Smith et al, 1991;Bianchi et al, 1995;Ezure, 1996).…”

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

“…As such, this population of neurons is thought to be solely premotor and has not been considered important in respiratory rhythmicity (see also Refs. 18,42,45). However, earlier studies also revealed that injection of the excitatory amino acid agonist D,L-homocysteic acid (DLH) into the region of cVRC induced abdominal muscle activation (10, 51), increased laryngeal muscle activity and blood pressure (51), and decreased inspiratory neuronal and motor activity, which frequently led to the complete apnea (10).…”