Elsevier

Brain Research

Volume 768, Issues 1–2, 12 September 1997, Pages 71-85
Brain Research

Research report
Role of respiratory and non-respiratory neurones in the region of the NTS in the elaboration of the sneeze reflex in cat

https://doi.org/10.1016/S0006-8993(97)00602-1Get rights and content

Abstract

Extracellular recordings were made in the dorsal respiratory group (DRG) and adjacent reticular formation following single-shock stimulation of the anterior ethmoidal nerve (AEN) and during sneeze evoked by repetitive stimulation of the AEN in nembutal-anaesthetized, curarized and ventilated cats. These neurones were characterised according to (i) their activity during the respiratory cycle (as inspiratory augmenting or decrementing (I Aug or I Dec), expiratory augmenting or decrementing (E Aug or E Dec), silent or tonic), and (ii) their axonal projection (bulbospinal or non-bulbospinal–non-vagal (BS or NBS–NV)). Following single-shock stimulation of the AEN, most of the inspiratory neurones were transiently inhibited, whereas E Aug neurones were activated and E Dec neurones were activated and then inhibited. Silent neurones responded with a multispike or a paucispike pattern. Following repetitive stimulation of the AEN and during the resulting sneeze reflex, I Aug neurones increased their activity in parallel with the phrenic activity, I Dec neurones fired at the onset and at the end of the inspiration, E Dec and some silent neurones fired either during the compressive phase or after the expulsive phase, whereas E Aug and some silent neurones fired during the expulsive phase. We conclude that sneeze involves a reconfiguration of the central respiratory drive which uses, at least partly, the respiratory network to trigger a non-ventilatory defensive motor act.

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)

  • J.M. Macron et al.

    Influence of vagal afferents in the sneeze reflex in cats

    Neurosci. Lett.

    (1994)
  • S. Ootani et al.

    Convergence of afferents from SLN and GPN in cat medullary swallowing neurons

    Brain Res. Bull.

    (1995)
  • J. Orem et al.

    The activity of retrofacial expiratory cells during behavioral respiratory responses and active expiration

    Brain Res.

    (1986)
  • R.J. Person

    Somatic and vagal afferent convergence on solitary tract neurons in cat: electrophysiological characteristics

    Neuroscience

    (1989)
  • W.M. Price et al.

    Respiratory neurons participating in sneeze and in responses to resistance to expiration

    Exp. Neurol.

    (1970)
  • B.J. Sessle et al.

    Effects of upper respiratory tract stimuli on respiration and single respiratory neurons in the adult cat

    Exp. Neurol.

    (1978)
  • R. Shannon

    Intercostal and abdominal muscle afferent influence on medullary dorsal respiratory group neurons

    Respir. Physiol.

    (1980)
  • S. Takagi et al.

    Convergence of laryngeal afferents with different natures upon cat NTS neurons

    Brain Res. Bull.

    (1995)
  • F. Wallois et al.

    Postnatal development of the anterior ethmoidal nerve in cats: unmyelinated and myelinated nerve fiber analysis

    Neurosci. Lett.

    (1993)
  • F. Wallois et al.

    Activities of vagal receptors in the different phases of sneeze in cats

    Respir. Physiol.

    (1995)
  • F. Wallois et al.

    Nasal air puff stimulations and laryngeal, thoracic and abdominal muscle activities

    Respir. Physiol.

    (1994)
  • F. Wallois et al.

    Trigeminal afferences implied in the triggering or inhibition of sneezing in cats

    Neurosci. Lett.

    (1991)
  • F. Wallois et al.

    Trigeminal nasal receptors related to respiration and to various stimuli in cats

    Respir. Physiol.

    (1991)
  • F. Wallois et al.

    Influence of trigeminal nasal afferents on bulbar respiratory neuronal activity

    Brain Res.

    (1992)
  • Y. Zheng et al.

    Are the post-inspiratory neurons in the decerebrate rat cranial motoneurons or interneurons?

    Brain Res.

    (1991)
  • J.C. Barillot et al.

    Study of the validity of the collision test. Application to the bulbo-spinal respiratory neurons

    J. Physiol. (Paris)

    (1980)
  • H.L. Batsel, Central nervous integration of defensive reflexes, in: I. Hutàs, L.A. Debreczeni (Eds.), Advances in...
  • H.L. Batsel et al.

    Neural mechanisms of sneeze

    Am. J. Physiol.

    (1975)
  • A.J. Berger et al.

    Lateralized phrenic nerve responses to stimulating respiratory afferents in the cat

    Am. J. Physiol.

    (1976)
  • Cited by (17)

    • The sigh and related behaviors

      2022, Handbook of Clinical Neurology
      Citation Excerpt :

      Sigh generation possibly shares neuronal mechanisms with yawning, hiccups, and sneezing and it is likely that the medulla is critical for the generation of these behaviors. The medulla seems to be sufficient for generating yawning in humans (Heusner, 1946; Argiolas and Melis, 1998), and in the case of sneezing, neuronal sneezing-associated activity has been recorded in central respiratory neurons in cats (Batsel and Lines, 1978; Jakus et al., 1985; Orem and Brooks, 1986; Wallois et al., 1997). The function of sneezing is well described, and like these other behaviors can also occur abnormally, such as in nonallergic rhinitis (Lieberman and Pattanaik, 2014; Agnihotri and McGrath, 2019).

    • Sneezing reflex is mediated by a peptidergic pathway from nose to brainstem

      2021, Cell
      Citation Excerpt :

      We therefore hypothesize that a specific population of postsynaptic neurons in the sneeze-evoking region mediates the sneezing reflex. Previous studies have shown that stimulation of nasal sensory fibers or ethmoidal nerve triggers sneezing in both cats and humans (Batsel and Lines, 1978; Geppetti et al., 1988; Hydén and Arlinger, 2007; Satoh et al., 1998; Taylor-Clark et al., 2005; Wallois et al., 1991, 1997). However, it remains unclear which population of nasal sensory neurons initiates the sneezing reflex and which neurotransmitters/neuropeptides in nasal sensory neurons are required for transmitting sneeze signals.

    • Central nervous mechanisms of cough

      2002, Pulmonary Pharmacology and Therapeutics
    • Physiology and pathophysiology of sneezing and itching: Mechanisms of the symptoms

      2023, Nasal Physiology and Pathophysiology of Nasal Disorders
    View all citing articles on Scopus
    View full text