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. 1991 Aug;439:545–558. doi: 10.1113/jphysiol.1991.sp018681

The cortical drive to human respiratory muscles in the awake state assessed by premotor cerebral potentials.

G Macefield 1, S C Gandevia 1
PMCID: PMC1180123  PMID: 1895244

Abstract

1. We investigated the possibility of a cortical contribution to human respiration by recording from the scalp of awake subjects the premotor cerebral potentials that are known to precede voluntary limb movements. 2. Electroencephalographic activity (EEG) was recorded from scalp electrodes and averaged for 1.8-2.0 s before the time at which airway pressure exceeded an inspiratory or expiratory threshold. Clear premotor cerebral potentials were recorded during brisk, self-paced nasal inhalations or exhalations. In ten subjects, a slow cortical negativity (Bereitschaftspotential) was apparent in the averaged EEG, commencing 1.2 +/- 0.3 s before the onset of inspiratory (scalene) or expiratory (abdominal) muscle activity (EMG). It was maximal at the vertex, with a mean slope of 12.3 +/- 5.8 microV/s, and was followed by a post-movement positivity. 3. In four subjects the inspiratory premotor potential culminated in a large negativity, the motor potential, which began 24 +/- 15 ms before the onset of scalene EMG. It is argued that such a short latency is consistent with a volitionally generated respiratory command which travels relatively directly to the respiratory muscles, having a total central delay which is no longer than that for voluntary finger movements. 4. That the respiratory premotor and motor potentials did not originate in subcortical structures was supported by their absence in a patient suffering from chronic reflexogenic hiccups, in whom cerebral activity was back-averaged from each brisk hiccup. 5. During quiet breathing, in which subjects were relaxed and distracted from thinking about their respiration, no premotor cerebral potentials preceding inspiration could be detected. This failure was not due to the slow rate of rise of inspiratory activity during quiet breathing as compared with a brisk sniff, because premotor potentials were detected when subjects intermittently generated slow active expiratory efforts. 6. These observations suggest that during quiet breathing the cerebral cortex does not contribute to respiratory drive on a breath-by-breath basis. Conversely, the presence of clear premotor cerebral potentials when subjects performed self-paced inspiratory or expiratory manoeuvres illustrates the powerful cortical projection to human respiratory muscles.

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Selected References

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  1. Adams L., Datta A. K., Guz A. Synchronization of motor unit firing during different respiratory and postural tasks in human sternocleidomastoid muscle. J Physiol. 1989 Jun;413:213–231. doi: 10.1113/jphysiol.1989.sp017650. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aminoff M. J., Sears T. A. Spinal integration of segmental, cortical and breathing inputs to thoracic respiratory motoneurones. J Physiol. 1971 Jun;215(2):557–575. doi: 10.1113/jphysiol.1971.sp009485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armstrong D. M. The supraspinal control of mammalian locomotion. J Physiol. 1988 Nov;405:1–37. doi: 10.1113/jphysiol.1988.sp017319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barrett G., Shibasaki H., Neshige R. Cortical potentials preceding voluntary movement: evidence for three periods of preparation in man. Electroencephalogr Clin Neurophysiol. 1986 Apr;63(4):327–339. doi: 10.1016/0013-4694(86)90017-9. [DOI] [PubMed] [Google Scholar]
  5. Bassal M., Bianchi A. L., Dussardier M. Effets de la stimulation des structures nerveuses centrales sur l'activité des neurones respiratoires chez le chat. J Physiol (Paris) 1981 Sep;77(6-7):779–795. [PubMed] [Google Scholar]
  6. Bassal M., Bianchi A. L. Effets de la stimulation des structures nerveuses centrales sur les actrivités respiratoires efférentes chez le chat. I. Réponses à la stimulation corticale. J Physiol (Paris) 1981 Sep;77(6-7):741–757. [PubMed] [Google Scholar]
  7. Boschert J., Deecke L. Cerebral potentials preceding voluntary toe, knee and hip movements and their vectors in human precentral gyrus. Brain Res. 1986 Jun 18;376(1):175–179. doi: 10.1016/0006-8993(86)90913-3. [DOI] [PubMed] [Google Scholar]
  8. Brunia C. H., Voorn F. J., Berger M. P. Movement related slow potentials. II. A contrast between finger and foot movements in left-handed subjects. Electroencephalogr Clin Neurophysiol. 1985 Feb;60(2):135–145. doi: 10.1016/0013-4694(85)90020-3. [DOI] [PubMed] [Google Scholar]
  9. Cohen M. I., Piercey M. F., Gootman P. M., Wolotsky P. Synaptic connections between medullary inspiratory neurons and phrenic motoneurons as revealed by cross-correlation. Brain Res. 1974 Dec 6;81(2):319–324. doi: 10.1016/0006-8993(74)90946-9. [DOI] [PubMed] [Google Scholar]
  10. Davenport P. W., Friedman W. A., Thompson F. J., Franzén O. Respiratory-related cortical potentials evoked by inspiratory occlusion in humans. J Appl Physiol (1985) 1986 Jun;60(6):1843–1848. doi: 10.1152/jappl.1986.60.6.1843. [DOI] [PubMed] [Google Scholar]
  11. Davies J. G., Kirkwood P. A., Sears T. A. The distribution of monosynaptic connexions from inspiratory bulbospinal neurones to inspiratory motoneurones in the cat. J Physiol. 1985 Nov;368:63–87. doi: 10.1113/jphysiol.1985.sp015846. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Deecke L., Scheid P., Kornhuber H. H. Distribution of readiness potential, pre-motion positivity, and motor potential of the human cerebral cortex preceding voluntary finger movements. Exp Brain Res. 1969;7(2):158–168. doi: 10.1007/BF00235441. [DOI] [PubMed] [Google Scholar]
  13. Duffin J., Lipski J. Monosynaptic excitation of thoracic motoneurones by inspiratory neurones of the nucleus tractus solitarius in the cat. J Physiol. 1987 Sep;390:415–431. doi: 10.1113/jphysiol.1987.sp016709. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Eldridge F. L. Maintenance of respiration by central neural feedback mechanisms. Fed Proc. 1977 Sep;36(10):2400–2404. [PubMed] [Google Scholar]
  15. FINK B. R., HANKS E. C., HOLADAY D. A., SHIH H. N. Monitoring of ventilation by integrated diaphragmatic electromyogram. Determination of carbon dioxide threshold in anesthetized man. J Am Med Assoc. 1960 Mar 26;172:1367–1371. doi: 10.1001/jama.1960.03020130025007. [DOI] [PubMed] [Google Scholar]
  16. FINK B. R. Influence of cerebral activity in wakefulness on regulation of breathing. J Appl Physiol. 1961 Jan;16:15–20. doi: 10.1152/jappl.1961.16.1.15. [DOI] [PubMed] [Google Scholar]
  17. Gandevia S. C., Applegate C. Activation of neck muscles from the human motor cortex. Brain. 1988 Aug;111(Pt 4):801–813. doi: 10.1093/brain/111.4.801. [DOI] [PubMed] [Google Scholar]
  18. Gandevia S. C., Macefield G. Projection of low-threshold afferents from human intercostal muscles to the cerebral cortex. Respir Physiol. 1989 Aug;77(2):203–214. doi: 10.1016/0034-5687(89)90007-8. [DOI] [PubMed] [Google Scholar]
  19. Gandevia S. C., McKenzie D. K., Plassman B. L. Activation of human respiratory muscles during different voluntary manoeuvres. J Physiol. 1990 Sep;428:387–403. doi: 10.1113/jphysiol.1990.sp018218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gandevia S. C., Plassman B. L. Responses in human intercostal and truncal muscles to motor cortical and spinal stimulation. Respir Physiol. 1988 Sep;73(3):325–337. doi: 10.1016/0034-5687(88)90054-0. [DOI] [PubMed] [Google Scholar]
  21. Gandevia S. C., Rothwell J. C. Activation of the human diaphragm from the motor cortex. J Physiol. 1987 Mar;384:109–118. doi: 10.1113/jphysiol.1987.sp016445. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Hilaire G., Monteau R. Connexions entre les neurones inspiratoires bulbaires et les motoneurones phréniques et intercostaux. J Physiol (Paris) 1976;72(8):987–1000. [PubMed] [Google Scholar]
  23. Kirkwood P. A., Sears T. A. Proceedings: Monosynaptic excitation of thoracic expiratory motoneurones from lateral respiratory neurones in the medulla of the cat. J Physiol. 1973 Oct;234(2):87P–89P. [PubMed] [Google Scholar]
  24. Kristeva R., Kornhuber H. H. Cerebral potentials related to the smallest human finger movement. Prog Brain Res. 1980;54:178–182. [PubMed] [Google Scholar]
  25. Lee B. I., Lüders H., Lesser R. P., Dinner D. S., Morris H. H., 3rd Cortical potentials related to voluntary and passive finger movements recorded from subdural electrodes in humans. Ann Neurol. 1986 Jul;20(1):32–37. doi: 10.1002/ana.410200107. [DOI] [PubMed] [Google Scholar]
  26. Lipski J., Bektas A., Porter R. Short latency inputs to phrenic motoneurones from the sensorimotor cortex in the cat. Exp Brain Res. 1986;61(2):280–290. doi: 10.1007/BF00239518. [DOI] [PubMed] [Google Scholar]
  27. Merrill E. G. The descending pathways from the lateral respiratory neurones in cats. J Physiol. 1971 Oct;218 (Suppl):82P–83P. [PubMed] [Google Scholar]
  28. Murphy K., Mier A., Adams L., Guz A. Putative cerebral cortical involvement in the ventilatory response to inhaled CO2 in conscious man. J Physiol. 1990 Jan;420:1–18. doi: 10.1113/jphysiol.1990.sp017898. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. NATHAN P. W. THE DESCENDING RESPIRATORY PATHWAY IN MAN. J Neurol Neurosurg Psychiatry. 1963 Dec;26:487–499. doi: 10.1136/jnnp.26.6.487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Neshige R., Lüders H., Shibasaki H. Recording of movement-related potentials from scalp and cortex in man. Brain. 1988 Jun;111(Pt 3):719–736. [PubMed] [Google Scholar]
  31. Obeso J. A., Rothwell J. C., Marsden C. D. Simple tics in Gilles de la Tourette's syndrome are not prefaced by a normal premovement EEG potential. J Neurol Neurosurg Psychiatry. 1981 Aug;44(8):735–738. doi: 10.1136/jnnp.44.8.735. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Orem J. Behavioral inspiratory inhibition: inactivated and activated respiratory cells. J Neurophysiol. 1989 Nov;62(5):1069–1078. doi: 10.1152/jn.1989.62.5.1069. [DOI] [PubMed] [Google Scholar]
  33. Orem J., Netick A. Behavioral control of breathing in the cat. Brain Res. 1986 Feb 26;366(1-2):238–253. doi: 10.1016/0006-8993(86)91301-6. [DOI] [PubMed] [Google Scholar]
  34. Papakostopoulos D., Cooper R., Crow H. J. Inhibition of cortical evoked potentials and sensation by self-initiated movement in man. Nature. 1975 Nov 27;258(5533):321–324. doi: 10.1038/258321a0. [DOI] [PubMed] [Google Scholar]
  35. Plassman B. L., Gandevia S. C. Comparison of human motor cortical projections to abdominal muscles and intrinsic muscles of the hand. Exp Brain Res. 1989;78(2):301–308. doi: 10.1007/BF00228901. [DOI] [PubMed] [Google Scholar]
  36. Rikard-Bell G. C., Bystrzycka E. K., Nail B. S. The identification of brainstem neurones projecting to thoracic respiratory motoneurones in the cat as demonstrated by retrograde transport of HRP. Brain Res Bull. 1985 Jan;14(1):25–37. doi: 10.1016/0361-9230(85)90174-1. [DOI] [PubMed] [Google Scholar]
  37. Rikard-Bell G. C., Törk I., Bystrzycka E. K. Distribution of corticospinal motor fibres within the cervical spinal cord with special reference to the phrenic nucleus: a WGA-HRP anterograde transport study in the cat. Brain Res. 1986 Jul 30;379(1):75–83. doi: 10.1016/0006-8993(86)90257-x. [DOI] [PubMed] [Google Scholar]
  38. Rothwell J. C., Thompson P. D., Day B. L., Dick J. P., Kachi T., Cowan J. M., Marsden C. D. Motor cortex stimulation in intact man. 1. General characteristics of EMG responses in different muscles. Brain. 1987 Oct;110(Pt 5):1173–1190. doi: 10.1093/brain/110.5.1173. [DOI] [PubMed] [Google Scholar]
  39. Shibasaki H., Barrett G., Halliday E., Halliday A. M. Components of the movement-related cortical potential and their scalp topography. Electroencephalogr Clin Neurophysiol. 1980 Aug;49(3-4):213–226. doi: 10.1016/0013-4694(80)90216-3. [DOI] [PubMed] [Google Scholar]
  40. Shibasaki H., Barrett G., Halliday E., Halliday A. M. Cortical potentials associated with voluntary foot movement in man. Electroencephalogr Clin Neurophysiol. 1981 Dec;52(6):507–516. doi: 10.1016/0013-4694(81)91426-7. [DOI] [PubMed] [Google Scholar]
  41. Shibasaki H., Barrett G., Halliday E., Halliday A. M. Cortical potentials following voluntary and passive finger movements. Electroencephalogr Clin Neurophysiol. 1980 Nov;50(3-4):201–213. doi: 10.1016/0013-4694(80)90147-9. [DOI] [PubMed] [Google Scholar]
  42. Shibasaki H., Sakai T., Nishimura H., Sato Y., Goto I., Kuroiwa Y. Involuntary movements in chorea-acanthocytosis: a comparison with Huntington's chorea. Ann Neurol. 1982 Sep;12(3):311–314. doi: 10.1002/ana.410120319. [DOI] [PubMed] [Google Scholar]
  43. Tarkka I. M., Hallett M. Cortical topography of premotor and motor potentials preceding self-paced, voluntary movement of dominant and non-dominant hands. Electroencephalogr Clin Neurophysiol. 1990 Feb;75(2):36–43. doi: 10.1016/0013-4694(90)90150-i. [DOI] [PubMed] [Google Scholar]

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