Frontiers Review
Brain, breathing and breathlessness

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Abstract

This review attempts to summarize: (i) evidence on how man voluntarily or behaviourally (as in speech) alters breathing; and (ii) evidence on how the breathlessness induced by CO2 inhalation, is perceived. The application of new methods to study these problems, e.g. functional brain imaging and transcranial focal brain stimulation, is summarized. Studies of patients with specific neurological lesions have shed considerable light in this area. The key requirement for the ponto-medullary respiratory oscillator to be both `intact' and `responsive' for the perception of CO2-induced air hunger is emphasized. We are ignorant as to how the voluntary/behavioural control system interacts with the automatic system at any site above the final common pathway of the respiratory anterior horn cells in the cervical and thoracic spinal cord. The opportunities for further work are outlined.

Section snippets

The neurology of automatic breathing

The objective of this presentation is to review recent experimental evidence in man on two separate but related subjects: (i) mechanisms underlying voluntary or behavioural control of breathing; and (ii) mechanisms underlying the sensation of breathlessness. In order to understand the story, it is necessary to examine Fig. 1.

Automatic breathing originates in the ponto-medullary respiratory oscillator from which a descending bulbo-spinal projection synapses with the anterior horn cells in the

Anatomy and physiology underlying voluntary/behavioural breathing

The schematic outline so far does not explain how man can take a breath at will, nor how expiratory airflow can be perfectly controlled to produce phonation. It also does not explain how emotions can affect breathing. Most importantly, it does not explain how breathing increases the `right amount' during exercise where there would appear to be no error signal to regulate breathing, in the absence of metabolic acidosis with more severe exercise. Such failure to explain essentially error-free

Imaging the brain to elucidate neuronal areas concerned with voluntary/behavioural breathing

Positron emission tomography (PET) allows the non-invasive measurement of regional cerebral blood flow and has been used to define areas of increased neural activity associated with specific motor tasks in conscious humans. Regional blood flow increases when regional O2 consumption increases, particularly in association with local increases in synaptic activity. This increase in blood flow can be `marked' by the use of isotopes that accumulate in such regions, following the distribution of

Is the motor cortex involved in breathing control during exercise?

We still cannot agree on why breathing increases on exercise! The question takes us back to the proposal of Krogh and Lindhard (1913)that motor cortical activation to exercising muscles might induce increases in breathing via irradiation of either brainstem respiratory centres (Fig. 1, see dotted lines from right corticospinal tract to pontomedullary oscillator) or of cortical areas controlling respiratory muscles. Could these cortical areas, described in Section 3, be shown to be active during

The `Curse of Ondine' and the `Locked-in Syndrome': clinical lessons

These studies provide some physiological basis for the voluntary/behavioural aspects of breathing as opposed to the automatic ponto-medullary breathing. Fig. 1 shows a dotted line from the left corticospinal tract for volitional breathing which represents a probable input into the respiratory oscillator. Experiments in the cat (Orem and Nettick, 1986; Orem, 1988) suggest that voluntary or behavioural influences are integrated within the brainstem areas that house the automatic ponto-medullary

The sensation of breathlessness; focus on `air hunger' induced by CO2

An up-to-date review of this subject has been published as a multi-author volume in 1996 (Adams and Guz, 1996). It would not be appropriate to summarize this here. Breathlessness is not a uniform sensation, it has many different qualities (Simon et al., 1990). I shall focus on the sensation of `air hunger' or the `urge to breathe'. This sensation typically occurs in subjects given carbon dioxide to breathe or made to exercise when breathing discomfort is further described by such phrases as

Focus on sensations induced from the lung

There is clear need to scan the brain for activations that are likely to occur with afferent vagal input from the lungs. This could include a study of the `raw' sensation in the chest provoked by irritating the airways and also the sensation that may be evoked by activation of c-fibres from the lung, as is likely to occur in pulmonary oedema. The difficulties of doing such studies would appear to be immense, but were they to be accomplished, richly rewarding.

Conclusion

We are at a very early stage in trying to understand how higher brain centres can control breathing and experience breathlessness in humans. New methods have now made these studies possible.

Acknowledgements

I am deeply grateful to my colleagues in the Department of Medicine at Charing Cross and Westminster Medical School (especially Professor Lewis Adams) and also to my colleagues at the MRC Cycloctron Unit, Royal Postgraduate Medical School, London, for their close interaction with me over many years. Thanks are also expressed to the Wellcome Trust for their generous financial support which made this work possible.

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