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Forebrain and Midbrain Influence on Respiration

André Hugelin

10.1002/cphy.cp030202

Source: Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing

Originally published: 1986

Published online: January 2011

Full Article on Wiley Online Library



Abstract

The sections in this article are:

1 Respiratory Effects of Stimulation
1.1 Inhibitory Effects
1.2 Excitatory Effects
2 Descending Pathways
2.1 Anatomical Studies
2.2 Electrophysiological Studies
2.3 Termination on Medullary Respiratory Neurons
2.4 Termination on Respiratory Motoneurons
3 Physiological Respiratory Adjustments
3.1 Tonic Respiratory Drive From Mesencephalon and Diencephalon
3.2 Cortical Inhibition
4 Respiratory Effects of Mental Activity
4.1 Thought, Attention, and Emotion
4.2 Voluntary Control of Respiration
5 Conclusion
Figure 1. Figure 1.

Respiratory inhibitory (top) and facilitatory (bottom) effects of electrical stimulation of cerebral cortex of cat. Rise in blood pressure (upper trace) was elicited by stimulation of inhibitory area of orbital gyrus. Respiratory acceleration was obtained from pericruciate gyrus (sensorimotor area).

From Smith 145. In: Journal of Neurophysiology, 1938. Courtesy of Charles C Thomas, Publisher, Springfield, Illinois
Figure 2. Figure 2.

Routes by which inhibitory pathways from area 13 reach mesencephalic tegmentum of cat.

From Turner 155
Figure 3. Figure 3.

Cat brain stem regions (stippled areas) from which stimulation produces excitation of respiration combined with electroencephalogram arousal and other concomitants of general alerting reaction. CGL, corpus geniculatus lateralis; CGM, corpus geniculatus medialis; CI, capsula interna; CP, commissura posterior; Cqa, corpus quadrigeminum anticum; Ddt, decussatio dorsalis tegmenti; Dvt, decussatio ventralis tegmenti; En, nucleus entopedoncularis; F, fornix; GP, globus pallidus; IP, ganglio interpedoncularis; Lm, lemniscus medialis; MD, nucleus medialis thalami; Mm, nucleus mammilaris medialis; Nc, nucleus caudatus; NR, nucleus ruber; P, pons; Ped, pes pedonculus; Put, putamen; PV, nucleus paraventricularis; R, nucleus reticulatus thalami; SN, substantia nigra; TO, tractus opticus; VA, nucleus anteroventralis thalami; ZI, zona incerta.

From Cohen and Hugelin 36
Figure 4. Figure 4.

Changes in phrenic pattern of discharge in response to mesencephalic reticular stimulation produced by modifying alveolar CO2 tension in curarized low encéphale isolé cat preparation. Respiratory patterns during reticular stimulation are identical in A, B, and C, but depending on prestimulation pattern, stimulation increases (A) or reduces (B, C) respiratory rate. , fractional concentration of CO2 in alveolar gas. Horizontal bars (c), duration of prestimulation control cycle.

From Cohen and Hugelin 36
Figure 5. Figure 5.

General arousal reaction on mesencephalic reticular stimulation in locally anesthetized, vagotomized, low encéphale isolé cat preparation. Note inhibition of polysynaptic jaw‐opening reflex (JOR), enhanced amplitude of integrated phrenic nerve discharge (Phr), and electrocorticogram (ECG) desynchronization. Repetitive electrical stimulation at 300 Hz delivered during time indicated by signal on bottom trace. Effects were maximum during 1st seconds of stimulation and decreased progressively to steady level in 2nd part. Steady level was attributed to cortical inhibitory influence because effects were suppressed by diencephalic transection.

From Hugelin and Cohen 83
Figure 6. Figure 6.

Comparison of cortical regions influencing respiration in cat. A: areas from which single shock evokes complex phrenic phasic response. Dots, dominant excitatory response; open circles, dominant inhibitory response; shaded area, intermediate response. B: topography of regions from which repetitive stimulation elicits inhibition (dots) or acceleration (lines). Closest stippling and lines, areas from which responses were most easily obtained.

A from Planche 125; B from Smith 145. In: Journal of Neurophysiology, 1938. Courtesy of Charles C Thomas, Publisher, Springfield, Illinois
Figure 7. Figure 7.

Different phrenic phasic responses to single‐shock cortical stimulation. A: dominant excitatory response on pericruciate excitation. B: dominant inhibitory response on orbital gyrus stimulation. C: intermediate response on stimulation of point between excitatory and inhibitory areas. Above each recording, 1‐4 designate successive excitatory responses. Identical responses were recorded homo‐ and contralaterally. Arrows indicate stimulation time.

Adapted from Planche 126
Figure 8. Figure 8.

Dissociation of bulbospinal respiratory drive mediated by crossed descending tract and reticulospinal facilitation mediated by direct pathway. A: spontaneous inspiratory electromyogram activity of left and right diaphragms and external and internal intercostal muscles. B: tonic discharge produced by stimulating medial gigantocellular reticular field at point indicated by dot A. C: after midline incision from C2 to obex, respiratory activity is suppressed on both sides, whereas reticular stimulation still produces tonic discharge of respiratory muscles through direct and crossed pathways left intact by limited midline incision.

From Sears 142
Figure 9. Figure 9.

Increase in respiratory rate (upper curves) and rectal temperature (lower curves) in response to external body warming. Filled circles, normal deep breaths; open circles, polypnea; crosses, panting (open mouth, moving jaw, and salivation). Top: intact cat. Bottom: 45 days after bilateral hypothalmic electrolytic lesion.

From Hess and Stoll 74
Figure 10. Figure 10.

Topography of hypothalamic region from which electrical stimulation elicits thermal polypnea and panting in goat. A: parasagittal section through preoptic area and hypothalamus. Cross‐hatched area, responsive region. B: frontal section through hypothalamus caudal to anterior commissure. Filled circles, points from which polypnea was elicited; open circles, points from which stimulation was ineffective. C.a., commissura anterior; C.f.d., columna fornicis descendens; Ch.o., chiasma opticum; C.m., corpus mammillare; Inf., infundibulum; P.C., pedunculus cerebri; V. d'A., tractus Vicq d'Azyr; 3, 3rd ventricle.

From Andersson et al. 6
Figure 11. Figure 11.

Effects on respiratory rate, ear surface temperature, and shivering of electrical stimulation of heat‐sensitive hypothalamic area of goat before and after body temperature was artificially lowered. Double line on lower curve indicates panting.

From Andersson et al. 6
Figure 12. Figure 12.

Inversion of inspiratory discharge pattern from slowly increasing type to slowly decreasing type during thermal polypnea. Top: phrenic discharge before (top trace) and during (bottom trace) hypothalamic heating. Bottom: inspiration‐triggered time histogram of bulbospinal neuron, recorded in ventral bulbar respiratory nucleus during normopnea (left) and during thermal polypnea (right).

Adapted from Dussardier et al. 47
Figure 13. Figure 13.

Phrenic discharge at different alveolar CO2 levels: A, 8.9%; B, 5.3%; C, 3.4%; D, 2.2%. Top traces, phrenic potentials after integration with resistance‐capacitance integrating circuit; bottom traces, directly recorded phrenic potentials.

From Cohen 34
Figure 14. Figure 14.

Schematic diagram of sagittal section of chronic cat brain showing region essential to decorticate panting (dotted area). Transection AA did not eliminate decorticate panting, which was suppressed after BB section. H, habenula; SC, superior colliculus; IC, inferior colliculus; OC, optic chiasma; CM, corpus mammilare; E, epiphysis.

From Lilienthal and Otenasek 96
Figure 15. Figure 15.

Different effects of hypoxia on ventilation (group mean) under conscious control conditions (filled symbols) and after decortication (open symbols). Partial pressure of O2 was controlled throughout hypoxia exposure at level indicated in parentheses. f, Respiratory frequency; VT, tidal volume; VE, expired minute ventilation; , alveolar partial pressure of O2.

From Tenney and Ou 152
Figure 16. Figure 16.

Schematic diagram of principal excitatory (+) and inhibitory (‐) pathways in hypoxic ventilatory control. PCR, peripheral chemoreceptor.

From Tenney et al. 153
Figure 17. Figure 17.

Effects of attention test on human cardiac frequency (FC), pneumotachograph (dV/dt), expired CO2 fraction (FEco2), tidal volume (VT), electrodermogram (EDG), and 3 electroencephalogram (EEG) traces. Instructions were given to subject at 1st mark of bottom trace, and task began at 2nd mark. OP, occipitoparietal lead; FF, frontofrontal lead.

From Gautier 166
Figure 18. Figure 18.

Electromyogram (EMG) of inspiratory and expiratory intercostal muscles during singing of a sustained tone (2 lower traces). Upper trace, airflow; 2nd trace, spirogram expressed as percent vital capacity (% VC).

From Sears and Newsom Davis 143


Figure 1.

Respiratory inhibitory (top) and facilitatory (bottom) effects of electrical stimulation of cerebral cortex of cat. Rise in blood pressure (upper trace) was elicited by stimulation of inhibitory area of orbital gyrus. Respiratory acceleration was obtained from pericruciate gyrus (sensorimotor area).

From Smith 145. In: Journal of Neurophysiology, 1938. Courtesy of Charles C Thomas, Publisher, Springfield, Illinois


Figure 2.

Routes by which inhibitory pathways from area 13 reach mesencephalic tegmentum of cat.

From Turner 155


Figure 3.

Cat brain stem regions (stippled areas) from which stimulation produces excitation of respiration combined with electroencephalogram arousal and other concomitants of general alerting reaction. CGL, corpus geniculatus lateralis; CGM, corpus geniculatus medialis; CI, capsula interna; CP, commissura posterior; Cqa, corpus quadrigeminum anticum; Ddt, decussatio dorsalis tegmenti; Dvt, decussatio ventralis tegmenti; En, nucleus entopedoncularis; F, fornix; GP, globus pallidus; IP, ganglio interpedoncularis; Lm, lemniscus medialis; MD, nucleus medialis thalami; Mm, nucleus mammilaris medialis; Nc, nucleus caudatus; NR, nucleus ruber; P, pons; Ped, pes pedonculus; Put, putamen; PV, nucleus paraventricularis; R, nucleus reticulatus thalami; SN, substantia nigra; TO, tractus opticus; VA, nucleus anteroventralis thalami; ZI, zona incerta.

From Cohen and Hugelin 36


Figure 4.

Changes in phrenic pattern of discharge in response to mesencephalic reticular stimulation produced by modifying alveolar CO2 tension in curarized low encéphale isolé cat preparation. Respiratory patterns during reticular stimulation are identical in A, B, and C, but depending on prestimulation pattern, stimulation increases (A) or reduces (B, C) respiratory rate. , fractional concentration of CO2 in alveolar gas. Horizontal bars (c), duration of prestimulation control cycle.

From Cohen and Hugelin 36


Figure 5.

General arousal reaction on mesencephalic reticular stimulation in locally anesthetized, vagotomized, low encéphale isolé cat preparation. Note inhibition of polysynaptic jaw‐opening reflex (JOR), enhanced amplitude of integrated phrenic nerve discharge (Phr), and electrocorticogram (ECG) desynchronization. Repetitive electrical stimulation at 300 Hz delivered during time indicated by signal on bottom trace. Effects were maximum during 1st seconds of stimulation and decreased progressively to steady level in 2nd part. Steady level was attributed to cortical inhibitory influence because effects were suppressed by diencephalic transection.

From Hugelin and Cohen 83


Figure 6.

Comparison of cortical regions influencing respiration in cat. A: areas from which single shock evokes complex phrenic phasic response. Dots, dominant excitatory response; open circles, dominant inhibitory response; shaded area, intermediate response. B: topography of regions from which repetitive stimulation elicits inhibition (dots) or acceleration (lines). Closest stippling and lines, areas from which responses were most easily obtained.

A from Planche 125; B from Smith 145. In: Journal of Neurophysiology, 1938. Courtesy of Charles C Thomas, Publisher, Springfield, Illinois


Figure 7.

Different phrenic phasic responses to single‐shock cortical stimulation. A: dominant excitatory response on pericruciate excitation. B: dominant inhibitory response on orbital gyrus stimulation. C: intermediate response on stimulation of point between excitatory and inhibitory areas. Above each recording, 1‐4 designate successive excitatory responses. Identical responses were recorded homo‐ and contralaterally. Arrows indicate stimulation time.

Adapted from Planche 126


Figure 8.

Dissociation of bulbospinal respiratory drive mediated by crossed descending tract and reticulospinal facilitation mediated by direct pathway. A: spontaneous inspiratory electromyogram activity of left and right diaphragms and external and internal intercostal muscles. B: tonic discharge produced by stimulating medial gigantocellular reticular field at point indicated by dot A. C: after midline incision from C2 to obex, respiratory activity is suppressed on both sides, whereas reticular stimulation still produces tonic discharge of respiratory muscles through direct and crossed pathways left intact by limited midline incision.

From Sears 142


Figure 9.

Increase in respiratory rate (upper curves) and rectal temperature (lower curves) in response to external body warming. Filled circles, normal deep breaths; open circles, polypnea; crosses, panting (open mouth, moving jaw, and salivation). Top: intact cat. Bottom: 45 days after bilateral hypothalmic electrolytic lesion.

From Hess and Stoll 74


Figure 10.

Topography of hypothalamic region from which electrical stimulation elicits thermal polypnea and panting in goat. A: parasagittal section through preoptic area and hypothalamus. Cross‐hatched area, responsive region. B: frontal section through hypothalamus caudal to anterior commissure. Filled circles, points from which polypnea was elicited; open circles, points from which stimulation was ineffective. C.a., commissura anterior; C.f.d., columna fornicis descendens; Ch.o., chiasma opticum; C.m., corpus mammillare; Inf., infundibulum; P.C., pedunculus cerebri; V. d'A., tractus Vicq d'Azyr; 3, 3rd ventricle.

From Andersson et al. 6


Figure 11.

Effects on respiratory rate, ear surface temperature, and shivering of electrical stimulation of heat‐sensitive hypothalamic area of goat before and after body temperature was artificially lowered. Double line on lower curve indicates panting.

From Andersson et al. 6


Figure 12.

Inversion of inspiratory discharge pattern from slowly increasing type to slowly decreasing type during thermal polypnea. Top: phrenic discharge before (top trace) and during (bottom trace) hypothalamic heating. Bottom: inspiration‐triggered time histogram of bulbospinal neuron, recorded in ventral bulbar respiratory nucleus during normopnea (left) and during thermal polypnea (right).

Adapted from Dussardier et al. 47


Figure 13.

Phrenic discharge at different alveolar CO2 levels: A, 8.9%; B, 5.3%; C, 3.4%; D, 2.2%. Top traces, phrenic potentials after integration with resistance‐capacitance integrating circuit; bottom traces, directly recorded phrenic potentials.

From Cohen 34


Figure 14.

Schematic diagram of sagittal section of chronic cat brain showing region essential to decorticate panting (dotted area). Transection AA did not eliminate decorticate panting, which was suppressed after BB section. H, habenula; SC, superior colliculus; IC, inferior colliculus; OC, optic chiasma; CM, corpus mammilare; E, epiphysis.

From Lilienthal and Otenasek 96


Figure 15.

Different effects of hypoxia on ventilation (group mean) under conscious control conditions (filled symbols) and after decortication (open symbols). Partial pressure of O2 was controlled throughout hypoxia exposure at level indicated in parentheses. f, Respiratory frequency; VT, tidal volume; VE, expired minute ventilation; , alveolar partial pressure of O2.

From Tenney and Ou 152


Figure 16.

Schematic diagram of principal excitatory (+) and inhibitory (‐) pathways in hypoxic ventilatory control. PCR, peripheral chemoreceptor.

From Tenney et al. 153


Figure 17.

Effects of attention test on human cardiac frequency (FC), pneumotachograph (dV/dt), expired CO2 fraction (FEco2), tidal volume (VT), electrodermogram (EDG), and 3 electroencephalogram (EEG) traces. Instructions were given to subject at 1st mark of bottom trace, and task began at 2nd mark. OP, occipitoparietal lead; FF, frontofrontal lead.

From Gautier 166


Figure 18.

Electromyogram (EMG) of inspiratory and expiratory intercostal muscles during singing of a sustained tone (2 lower traces). Upper trace, airflow; 2nd trace, spirogram expressed as percent vital capacity (% VC).

From Sears and Newsom Davis 143
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Article Title: Forebrain and Midbrain Influence on Respiration
 

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André Hugelin. Forebrain and Midbrain Influence on Respiration. Compr Physiol 2011, Supplement 11: Handbook of Physiology, The Respiratory System, Control of Breathing: 69-91. First published in print 1986. doi: 10.1002/cphy.cp030202