In vitro studies of the carotid rete mirabile of artiodactyla

doi:10.1016/0026-2862(87)90013-6

Microvascular Research

Volume 33, Issue 2, March 1987, Pages 143-154

https://doi.org/10.1016/0026-2862(87)90013-6 Get rights and content

Abstract

The carotid rete of Artiodactyla, an intracranial arterial plexus which supplies blood to the brain, has intrigued investigators for a long time. This study was designed to examine the responsiveness of isolated retial arteries (250–700 μm in external diameter) of goat, pig, and cattle. The findings in these arteries were compared to those observed in cerebral arteries (250–650 μm in external diameter) of the same animal species. The magnitude of the arterial responses to potassium chloride varied with the resting tension applied to the tissue. The two types of vessels exhibited similar resting tension values (0.3 g) for maximal tension development in response to potassium chloride; however, the ability of retial vessels to contract in the presence of potassium chloride was consistently smaller than that of cerebral arteries. The contractile response of retial arteries to norepinephrine (10⁻⁹ to 10⁻⁴M), tyramine (10⁻⁸ to 10⁻³M), and field electrical stimulation (2–16 Hz) was negligible. The same retial arteries exhibited dose-dependent contractions in response to 5-hydroxytryptamine (10⁻⁹ to 10⁻⁵M) and histamine (10⁻⁹ to 3 × 10⁻⁴M). Cerebral arteries exhibited larger responses to the vasoactive agents than retial arteries. Our findings indicate that retial arteries have a small vasomotor activity in response to adrenergic stimulation or to vasoactive agents. Therefore, the carotid rete of Artiodactyla may have a low ability to change resistance to blood flow under neural or hormonal influences.

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Cited by (16)

Physical and computational fluid dynamics models for the hemodynamics of the artiodactyl carotid rete
2015, Journal of Theoretical Biology
Citation Excerpt :
These results imply that there are few sympathetic nerve endings and a paucity of catecholamine receptors in the arterial walls of the carotid rete itself. In artiodactyls, the result of sympathetic activity on intracranial blood flow is nearly identical to that of mammals with an ICA (Dieguez et al., 1983, 1987, 1988; Lluch et al., 1984), however, altered resistance is due to contraction of the cerebral arteries alone. Another mechanism for control of cerebral blood pressure is the presence of baroreceptor cells in the carotid sinus.
In the mammalian order Artiodactyla, the majority of arterial blood entering the intracranial cavity is supplied by a large arterial meshwork called the carotid rete. This vascular structure functionally replaces the internal carotid artery. Extensive experimentation has demonstrated that the artiodactyl carotid rete drives one of the most effective selective brain cooling mechanisms among terrestrial vertebrates. Less well understood is the impact that the unique morphology of the carotid rete may have on the hemodynamics of blood flow to the cerebrum. It has been hypothesized that, relative to the tubular internal carotid arteries of most other vertebrates, the highly convoluted morphology of the carotid rete may increase resistance to flow during extreme changes in cerebral blood pressure, essentially protecting the brain by acting as a resistor. We test this hypothesis by employing simple and complex physical models to a 3D surface rendering of the carotid rete of the domestic goat, Capra hircus. First, we modeled the potential for increased resistance across the carotid rete using an electrical circuit analog. The extensive branching of the rete equates to a parallel circuit that is bound in series by single tubular arteries, both upstream and downstream. This method calculated a near-zero increase in resistance across the rete. Because basic equations do not incorporate drag, shear–stress, and turbulence, we used computational fluid dynamics to simulate the impact of these computationally intensive factors on resistance. Ultimately, both simple and complex models demonstrated negligible changes in resistance and blood pressure across the arterial meshwork. We further tested the resistive potential of the carotid rete by simulating blood pressures known to occur in giraffes. Based on these models, we found resistance (and blood pressure mitigation as a whole) to be an unlikely function for the artiodactyl carotid rete.
The toadfish serotonin 2A (5-HT<inf>2A</inf>) receptor: Molecular characterization and its potential role in urea excretion
2012, Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology
Citation Excerpt :
The swim bladder was stripped of its skeletal muscle, so the 5-HT2A receptor that has been shown to be present in rat skeletal muscle (Guillet-Deniau et al., 1997; Hajduch et al., 1999) should be of no consequence. The gas gland and associated rete mirabile were likely included in the swim bladder preparation (Fänge and Wittenberg, 1958), and so elevated toadfish 5-HT2A receptor transcript may be present in that capacity as rete mirabile in both mammals and fish have been shown to respond to 5-HT (Myhre et al., 1976; Diéguez et al., 1987). However, we believe that the exceedingly high levels of transcript in the swim bladder, in addition to elevations in gonad and the hindbrain, may suggest a larger role for 5-HT2A in the toadfish, as all three of these regions are in fact interrelated in this fish.
Based on early pharmacological work, the serotonin 2A (5-HT_2A) receptor subtype is believed to be involved in the regulation of toadfish pulsatile urea excretion. The goal of the following study was to characterize the toadfish 5-HT_2A receptor at a molecular level, to determine the tissues in which this receptor is predominantly expressed and to further investigate the pharmacological specificity of toadfish pulsatile urea excretion by examining the effect of ketanserin, a 5-HT_2A receptor antagonist, on resting rates of pulsatile urea excretion. The full-length toadfish 5-HT_2A receptor encodes a 496 amino acid sequence and shares 57–80% sequence identity to 5-HT_2A receptors of other organisms, with 100% conservation among important ligand-binding residues. Toadfish 5-HT_2A receptor mRNA expression was highest in the swim bladder and gonad, followed by the whole brain. All other tissues tested (esophagus, stomach, anterior intestine, posterior intestine, rectum, liver, kidney, heart, muscle and gill) had mRNA expression levels that were significantly less than whole brain. Toadfish 5-HT_2A receptor mRNA expression within the brain was highest in the hindbrain, telencephalon and midbrain/diencephalon regions. Treatment with the 5-HT_2A receptor antagonist, ketanserin, resulted in a significant decrease in the pulsatile component of spontaneous urea excretion due to a reduction in urea pulse size with no significant change in pulse frequency. These results lend further support for the 5-HT_2A receptor in the regulation of pulsatile urea excretion in toadfish.
Innervation of cerebral arteries by nerves containing 5-hydroxytryptamine and noradrenaline
1995, Pharmacology and Therapeutics
Noradrenaline (NA)-containing nerves, mainly originating in the sympathetic superior cervical ganglia, supply large and small cerebral arteries. In large cerebral arteries, nerves containing serotonin (5-hydroxytryptamine, 5-HT) may represent neuronal uptake of circulating 5-HT by sympathetic nerves. 5-HT-containing nerves supplying small pial vessels probably have a central origin in the dorsal raphe nucleus. In most species, NA is a weak vasoconstrictor (α₁- or α₂-adrenoceptors), while 5-HT is a potent vasoconstrictor (5-HT₂ or 5-HT₁-like receptors) of large cerebral arteries. In contrast, both NA and 5-HT tend to cause vasodilatation in small pial vessels and arterioles. Adrenergic and serotonergic transmission can be modulated by pH, a range of putative neurotransmitters and neuromodulators, and by the endothelium. Sumatriptan, a 5-HT₁-like receptor agonist, has been shown to be effective in the treatment of migraine. Changes in NA- or 5-HT-containing nerves and/or in the responses of cerebral vessels to NA and 5-HT have been observed in a variety of vascular disorders, including cerebral vasospasm following subarachnoid haemorrhage, hypertension, and atherosclerosis.
Ca<sup>2+</sup> entry blockers inhibit prostaglandin F<inf>2+</inf>-induced cerebrovascular contractile responses In goats
1991, European Journal of Pharmacology
We examined the effects of extracellular Ca²⁺ withdrawal and of Ca²⁺ entry blockers on goat cerebrovascular responses to prostaglandin F_2α (PGF_2α). We measured isometric tension in isolated middle cerebral arteries, and cerebral blood flow (CBF) in unanesthetized animals. PGF_2α produced concentration-dependent contractions of isolated arteries. The contractions were partially inhibited by incubation in Ca²⁺-free medium (by 63.1 ± 1.8% without ethyleneglycol-bis-(β-amino-ethylether)-N,N,N', N'-tetra-acetate (EGTA), and by 82.4 ± 3.7% with EGTA). The Ca²⁺ entry blockers inhibited PGF_2α-elicited contraction and relaxed PGF_2α-precontracted arteries (nicardipine, 91.4 ± 9.8%; nimodipine, 73.1 ± 2.0%; and verapamil, 50.5 ± 4.5% relaxation of the active tone). Injection of PGF_2α into the cerebral circulation produced dose-dependent reductions in CBF (34.4 ± 2.1% after 30 μg) which were inhibited during infusion of Ca²⁺ entry blockers (nicardipine 10 μg/min, 14.7 ± 1.5%; nimodipine 10 μg/min, 13.6 ± 1.3%; and verapamil 100 μ/min, 13.7 ± 2.3% of flow reduction). We conclude that PGF_2α-elicited contraction of goat cerebral arteries is mainly mediated by extracellular Ca²⁺ influx through Ca²⁺ channels sensitive to Ca²⁺ entry blockers. The anticonstrictor effects of Ca²⁺ entry blockers observed in vitro are consistent with their inhibitory effect on the PGFz_2α-induced CBF reductions.
Mechanics of arteries forming the carotid rete of goat and cattle
1989, Microvascular Research
To determine the mechanics of arteries forming the carotid rete mirabile of goat and cattle, the wall tension-circumference length relationship was recorded isometrically in isolated retial arteries of 350–600 μm in external diameter under relaxed and potassium-activated conditions. The results are compared to those of pial arteries of similar size. In relaxed retial and cerebral vessels, tension-length relationship had nonlinear characteristics and the incremental elastic modulus rose as the circumference length increased, the modulus being lower in retial than in pial arteries. However, the stiffness of the artery considered as a whole (stiffness parameter β) was similar in the two types of vessels. In activated arteries, force development was a function of length and the magnitude of the response increased until an optimal length was reached after which the response decreased with further stretch. In all stretches studied the developed force was much lower in retial arteries. The calculated active stress at the various lengths was also smaller in retial than in cerebral arteries and the maximum active stress for retial arteries was about 30–50% of that for cerebral arteries. Therefore, the passive mechanical properties of retial arteries closely resemble those of cerebral arteries but retial arteries have a small contractility. This suggests that the carotid rete mirabile of Artiodactyla has a minor role in actively controlling blood supply to the brain. Comments on the hemodynamic significance of the carotid rete are included.
Brain blood supply in ruminants
2019, Medycyna Weterynaryjna

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In vitro studies of the carotid rete mirabile of artiodactyla

Abstract

Respir. Physiol.

Brain Res.

Life Sci.

The carotid sinus and the cerebral circulation

An anatomical, experimental and clinical investigation, including some observations on rete mirabile caroticum

Acta Phychiatr. Neurol.

Influence of the carotid rete on brain temperature in cats exposed to hot environments

J. Physiol. (London)

The influence of the nasal mucosa and the carotid rete upon hypothalamic temperature in sheep

J. Physiol. (London)

Variations in adrenergic innervation and contractile responses of the rabbit saphenous artery

Circ. Res.

Vascular contraction: Effect of age and extracellular calcium

Blood Vessels

Adrenergic vasoconstriction of the goat middle cerebral artery

Amer. J. Physiol.

Catecholamine content and response to norepinephrine of middle cerebral artery

Studies of the carotid rete and its associated arteries

Philos. Trans. R. Soc. London

Analysis of the cerebrovascular effects of 5-hydroxytryptamine in unanesthetized goats

J. Pharmacol. Exp. Ther.

Control of cerebral blood flow in the goat; role of the carotid rete

Amer. J. Physiol.

Reactions of strips of rabbit aorta to epinephrine, isopropylarterenol, sodium nitrite and other drugs

J. Pharmacol. Exp. Ther.

Constrictor and compliance responses of some arteries to nerve or drug stimulation

J. Physiol. (London)

Histomorphologic structure of the carotid rete-cavernous sinus complex and its functional importance in sheep (Ovis aries)

Amer. J. Vet. Res.