The concept of coupling blood flow to brain function: Revision required?

A tight coupling exists between brain function and cerebral perfusion in most situations. The Roy and Sherrington hypothesis has been widely accepted to account for the phenomenon: Increased neuronal metabolic activity will give rise to the accumulation of vasoactive catabolites, which decrease vascular resistance and thereby increase blood flow until normal homeostasis is reestablished. However, the hypothesis does not account for the disproportionate increase in flow that occurs in a number of circumstances. There are additional difficulties in reconciling more recent experimental data with the Roy and Sherrington hypothesis. In this review we direct attention toward the rich perivascular nerve supply to all parts of the cerebral circulation as possibly being an alternative control system allowing for rapid parallel changes in flow and neuronal activity.

[1]  J. Keller,et al.  Origin of fibers innervating the basilar artery of the cat , 1985, Neuroscience Letters.

[2]  L. Edvinsson,et al.  Pharmacological characterization of GABA receptors mediating vasodilation of cerebral arteries in vitro , 1979, Brain Research.

[3]  L. Edvinsson Functional role of perivascular peptides in the control of cerebral circulation , 1985, Trends in Neurosciences.

[4]  J. Olesen The effect of intracarotid epinephrine, norepinephrine, and angiotensin on the regional cerebral blood flow in man , 1972, Neurology.

[5]  L. Edvinsson,et al.  Pharmacological Analysis of 5‐Hydroxytryptamine Receptors in Isolated Intracranial and Extracranial Vessels of Cat and Man , 1978, Circulation research.

[6]  L. Edvinsson,et al.  Effect of the GABA receptor agonist muscimol on regional cerebral blood flow in the rat , 1980, Brain Research.

[7]  J. Reinhard,et al.  Serotonin neurons project to small blood vessels in the brain. , 1979, Science.

[8]  E. Mackenzie,et al.  Cerebral circulatory and metabolic effects of 5‐hydroxytryptamine in anesthetized baboons. , 1977, The Journal of physiology.

[9]  J. Mcculloch,et al.  The effects of the GABAergic agonist muscimol upon the relationship between local cerebral blood flow and glucose utilization , 1983, Brain Research.

[10]  B. K. Hartman,et al.  Ultrastructural evidence for central monoaminergic innervation of blood vessels in the paraventricular nucleus of the hypothalamus , 1977, Brain Research.

[11]  C. Sherrington,et al.  On the Regulation of the Blood‐supply of the Brain , 1890, The Journal of physiology.

[12]  W. Penfield,et al.  CEREBRAL VASODILATOR NERVES AND THEIR PATHWAY FROM THE MEDULLA OBLONGATA: WITH OBSERVATIONS ON THE PIAL AND INTRACEREBRAL VASCULAR PLEXUS , 1932 .

[13]  Effect of Topical Adenosine Deaminase Treatment on the Functional Hyperemic and Hypoxic Responses of Cerebrocortical Microcirculation , 1984, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  H. Winn,et al.  Changes in Brain Adenosine during Bicuculline‐Induced Seizures in Rats: Effects of Hypoxia and Altered Systemic Blood Pressure , 1980, Circulation research.

[15]  L. Edvinsson,et al.  Influence of serotinin and norepinephrine on flow capacity/pressure characteristics of feline isolated cerebral arteries. , 1986, Stroke.

[16]  N Kageyama,et al.  Gamma-aminobutyric acid-induced contraction of the dog basilar artery. , 1984, Pharmacology.

[17]  R Rubio,et al.  Relationship between adenosine concentration and oxygen supply in rat brain. , 1975, The American journal of physiology.

[18]  L. Sokoloff,et al.  Influence of γ-Hydroxybutyrate on the Relationship between Local Cerebral Glucose Utilization and Local Cerebral Blood Flow in the Rat Brain , 1985, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[19]  L. Edvinsson Sympathetic control of cerebral circulation , 1982, Trends in Neurosciences.

[20]  M. Moskowitz,et al.  Perivascular meningeal projections from cat trigeminal ganglia: possible pathway for vascular headaches in man. , 1981, Science.

[21]  C. Iadecola,et al.  Global Cerebral Vasodilatation Elicited by Focal Electrical Stimulation within the Dorsal Medullary Reticular Formation in Anesthetized Rat , 1983, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[22]  E. Dóra Adenosine and Hypoxic Vasodilatation , 1985, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[23]  S. Kety,et al.  THE GASEOUS METABOLISM OF THE BRAIN OF THE MONKEY , 1945 .

[24]  E. Mackenzie,et al.  Influence of endogenous norepinephrine on cerebral blood flow and metabolism. , 1976, American Journal of Physiology.

[25]  B. Siesjö,et al.  Influence of intravenously administered catecholamines on cerebral oxygen consumption and blood flow in the rat. , 1978, Acta physiologica Scandinavica.

[26]  H. Vidrio,et al.  On the mechanism of the coronary dilator effect of serotonin in the dog. , 1976, European journal of pharmacology.

[27]  D. Duverger,et al.  Central serotonergic nerves project to the pial vessels of the brain , 1983, Nature.

[28]  N. Lassen,et al.  The luxury-perfusion syndrome and its possible relation to acute metabolic acidosis localised within the brain. , 1966, Lancet.

[29]  B. Siesjö,et al.  Cerebral functional, metabolic and circulatory effects of intravenous infusion of adrenaline in the rat , 1980, Brain Research.

[30]  E. Betz ADAPTION OF REGIONAL CEREBRAL BLOOD FLOW IN ANIMALS EXPOSED TO CHRONIC ALTERATIONS OF pO2 AND pCO2 , 1965, Acta neurologica Scandinavica. Supplementum.

[31]  N. Toda,et al.  Responsiveness of Isolated Cerebral and Peripheral Arteries to Serotonin, Norepinephrine, and Transmural Electrical Stimulation , 1973, Circulation research.

[32]  E. Mackenzie,et al.  Effects of 5‐hydrooxytryptamine on pial arteriolar calibre in anaesthetized cats , 1977, The Journal of physiology.

[33]  F. Eckenstein,et al.  Two types of cholinergic innervation in cortex, one co-localized with vasoactive intestinal polypeptide , 1984, Nature.

[34]  L. Edvinsson,et al.  Pharmacological Characterization of Adrenergic Alpha and Beta Receptors Mediating the Vasomotor Responses of Cerebral Arteries Ir Vitro , 1974, Circulation research.

[35]  S. Shibata,et al.  γ‐AMINOBUTYRIC ACID RECEPTOR ON VASCULAR SMOOTH MUSCLE OF DOG CEREBRAL ARTERIES , 1975, British journal of pharmacology.

[36]  J. Bevan,et al.  Distribution and origins of VIP-immunoreactive nerves in the cephalic circulation of the cat , 1984, Peptides.

[37]  G. Glick,et al.  Evidence for the Direct Effect of Adrenergic Drugs on the Cerebral Vascular Bed of the Unanesthetized Goat , 1973, Stroke.

[38]  C. Iadecola,et al.  Electrical stimulation of cerebellar fastigial nucleus increases cerebral cortical blood flow without change in local metabolism: Evidence for an intrinsic system in brain for primary vasodilation , 1983, Brain Research.

[39]  D. Jacobowitz,et al.  Origin of cholinergic nerves to the rat major cerebral arteries: Coexistence with vasoactive intestinal polypeptide , 1985, Brain Research Bulletin.

[40]  M E Raichle,et al.  Correlation Between Regional Cerebral Blood Flow and Oxidative Metabolism: In Vivo Studies in Man , 1976 .

[41]  M. Purves,et al.  Observations on the Control of Cerebral Blood Flow in the Sheep Fetus and Newborn Lamb , 1969, Circulation research.

[42]  M. Moskowitz,et al.  Co‐localization of retrogradely transported wheat germ agglutinin and the putative neurotransmitter substance P within trigeminal ganglion cells projecting to cat middle cerebral artery , 1984, The Journal of comparative neurology.

[43]  N. Lassen,et al.  Cerebral blood flow and oxygen consumption in man. , 1959, Physiological reviews.

[44]  E. Rubinstein,et al.  The Electroencephalogram, Blood Flow, and Oxygen Uptake in Rabbit Cerebrum , 1981, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[45]  C. Estrada,et al.  GABA receptors mediate cerebral vasodilation in the unanesthetized goat , 1984, Brain Research.

[46]  B. Siesjö,et al.  Circulatory and metabolic effects in the brain induced by amphetamine sulphate. , 1978, Acta physiologica Scandinavica.

[47]  W. Kuschinsky,et al.  Local chemical and neurogenic regulation of cerebral vascular resistance. , 1978, Physiological reviews.

[48]  M. Raichle,et al.  Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[49]  M. Fujishima,et al.  Mechanisms of cerebral vasodilatation in hypoxia. , 1970, Transactions of the American Neurological Association.

[50]  D. Ingvar “Hyperfrontal” distribution of the cerebral grey matter flow in resting wakefulness; on the functional anatomy of the conscious state , 1979, Acta neurologica Scandinavica.

[51]  J. Severinghaus,et al.  Cerebral Intracellular Changes during Supercarbia: An in vivo 31P Nuclear Magnetic Resonance Study in Rats , 1985, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[52]  J. Mckee,et al.  Neurogenic Cerebral Vasodilation From Electrical Stimulation of the Cerebellum in the Monkey , 1976, Stroke.

[53]  J. Phillis,et al.  Adenosine Deaminase Inhibitors Enhance Cerebral Anoxic Hyperemia in the Rat , 1985, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[54]  R. Armstrong,et al.  Muscle blood flow patterns during exercise in partially curarized rats. , 1985, Journal of applied physiology.

[55]  W. Kuschinsky,et al.  Perivascular Potassium and pH as Determinants of Local Pial Arterial Diameter in Cats: A MICROAPPLICATION STUDY , 1972, Circulation research.