Research reportRole of respiratory and non-respiratory neurones in the region of the NTS in the elaboration of the sneeze reflex in cat
Introduction
Sneeze is the most powerful defensive reflex exhibited by the respiratory tract [31]. It is triggered by stimulation of nasal afferents, which pass mainly via the anterior ethmoidal nerve (AEN) 56, 58, and is finely shaped by vagal afferent inputs 33, 54. It involves an increased inspiration immediately followed by a brief enhanced expiration 31, 55. The thoraco-abdominal inspiratory and expiratory muscles and the laryngeal musculature have their activity drastically modified in the course of sneezing [55]. Using Fos-like immunoreactivity, neurones activated during sneeze can be identified in all the brainstem areas devoted to breathing control [53]. Thus, the entire network involved in respiration is likely to participate in the elaboration of sneezing and, moreover, sneeze can be regarded as a model of the adaptation of the central respiratory network to a non-ventilatory motor act. We have previously demonstrated that sneeze results at least partly from the activation of bulbospinal respiratory neurones of the ventral respiratory group (VRG) [58]. However, previous electrophysiological data [2] and the pattern of Fos-like expression [53] suggest that neurones located in the dorsal respiratory group (DRG) also participate in the sneeze reflex. The present study aimed to characterise the effect on the activity of neurones located in the nucleus tractus solitarius and adjacent reticular formation of nasal afferent stimulation using single shocks or the type of repetitive stimulation that elicits sneeze. Moreover, as vagal afferents shape the sneeze reflex, we also studied the effect of stimulation of vagal afferents on the activity of the neurones that responded to nasal stimulation. We hypothesised that the elaboration of the motor pattern driving the respiratory muscles during sneeze could result from the participation of respiratory and also non-respiratory neurones. Thus, we studied the effect of nasal stimulation on different respiratory-related neuronal populations (bulbospinal and non-bulbospinal–non-vagal neurones) and on non-respiratory neurones in the area of the DRG which encompasses the ventrolateral part of the nucleus tractus solitarius rostral to the obex, where inspiratory bulbospinal neurones are located 8, 50 and to which somatosensory afferents project (superior laryngeal nerve, chorda tympani, lingual and glossopharyngeal nerves) 22, 25, 36, 39, 40, 47.
Section snippets
Surgical procedures (Fig. 1)
Experiments were performed on 18 cats of either sex, weighing between 2.0 and 3.7 kg. Cats were sedated with halothane and further anaesthetised with sodium pentobarbital (pentobarbital: 17.5 mg/kg i.v.). The level of anaesthesia was carefully evaluated throughout the experiment and additional doses of anaesthetics were administrated intravenously (pentobarbital 3.5 mg/kg) whenever nociceptive stimuli elicited an increase in phrenic discharge, an enhancement of respiratory frequency or an
Electrical single-shock stimulation of AEN
The effect was studied of AEN stimulation on phrenic and intercostal nerve activities and on the activity of medullary units.
Phrenic nerve responses to AEN stimulation
AEN stimulation evoked a transient inhibition of phrenic nerve activity with a 10.2±2.5 ms delay (n=140). In some tests, phrenic inhibition was followed by a sharp increase in both the number and amplitude of complex phrenic nerve potentials.
Classification of the recorded neurones according to their pattern of discharge in eupnea
As indicated in Table 1, we recorded 71 strictly phasic inspiratory neurones, 6 tonic inspiratory modulated neurones, 7 expiratory
Discussion
The present study provides a comparative analysis of the firing pattern of individual neurones located within the dorsal respiratory group under different conditions of nasal afferent stimulation. Using single-shock stimulation, we demonstrated that nasal inputs affected the whole range of respiratory neurones that could be identified and also activated non-respiratory neurones. Using vagal stimulation, we identified neurones receiving a convergent input from nasal and vagal afferents. Using
Acknowledgements
We are greatly indebted to Mrs. F. Dusaussoy and F. Gros for technical assistance and iconography. Style and language were checked by Dr. R. Timms.
References (59)
- et al.
Discharge of respiratory neurons in sneeze resulting from ethmoidal nerve stimulation
Exp. Neurol.
(1978) Dorsal respiratory group neurons in the medulla of cat: spinal projections, responses to lung inflation and superior laryngeal nerve stimulation
Brain Res.
(1977)- et al.
Convergence of multiple sensory inputs onto neurons in the dorsolateral medulla in cats
Neuroscience
(1995) - et al.
Dorsal medullary inspiratory neurons: effects of superior laryngeal afferent stimulation
Brain Res.
(1989) - et al.
Effects of contralateral superior laryngeal nerve stimulation on dorsal medullary inspiratory neurons
Brain Res.
(1989) Synaptic connections between medullary respiratory neurons and considerations on the genesis of the respiratory rhythm
Prog. Neurobiol.
(1990)- et al.
Location and axonal projection of early-onset decrementing expiratory neurons in the cat
Neurosci. Lett.
(1993) - et al.
Synaptic inputs to medullary respiratory neurons from superior laryngeal afferents in the cat
Brain Res.
(1992) - et al.
Types and locations of respiratory-related neurons in lateral tegmental field of cat medulla oblongata
Brain Res.
(1984) - et al.
Phrenic to phrenic inhibition and excitation in spinal cats
Neurosci. Lett.
(1988)
Influence of vagal afferents in the sneeze reflex in cats
Neurosci. Lett.
Convergence of afferents from SLN and GPN in cat medullary swallowing neurons
Brain Res. Bull.
The activity of retrofacial expiratory cells during behavioral respiratory responses and active expiration
Brain Res.
Somatic and vagal afferent convergence on solitary tract neurons in cat: electrophysiological characteristics
Neuroscience
Respiratory neurons participating in sneeze and in responses to resistance to expiration
Exp. Neurol.
Effects of upper respiratory tract stimuli on respiration and single respiratory neurons in the adult cat
Exp. Neurol.
Intercostal and abdominal muscle afferent influence on medullary dorsal respiratory group neurons
Respir. Physiol.
Convergence of laryngeal afferents with different natures upon cat NTS neurons
Brain Res. Bull.
Postnatal development of the anterior ethmoidal nerve in cats: unmyelinated and myelinated nerve fiber analysis
Neurosci. Lett.
Activities of vagal receptors in the different phases of sneeze in cats
Respir. Physiol.
Nasal air puff stimulations and laryngeal, thoracic and abdominal muscle activities
Respir. Physiol.
Trigeminal afferences implied in the triggering or inhibition of sneezing in cats
Neurosci. Lett.
Trigeminal nasal receptors related to respiration and to various stimuli in cats
Respir. Physiol.
Influence of trigeminal nasal afferents on bulbar respiratory neuronal activity
Brain Res.
Are the post-inspiratory neurons in the decerebrate rat cranial motoneurons or interneurons?
Brain Res.
Study of the validity of the collision test. Application to the bulbo-spinal respiratory neurons
J. Physiol. (Paris)
Neural mechanisms of sneeze
Am. J. Physiol.
Lateralized phrenic nerve responses to stimulating respiratory afferents in the cat
Am. J. Physiol.
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