Skip to main content
Log in

Brain cooling in humans — anatomical considerations

  • Review Article
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Abstract

Vascular arrangements allowing a bulky transfer of venous blood from the skin of the head and from nasal and paranasal mucous membranes to the dura mater provide an excellent anatomical basis for the convection process of cooling, caused by evaporation of sweat or mucus. The dura mater, with its extraordinarily high vascularization controlled by a potent vasomotor apparatus, may transmit temperature changes to the cerebrospinal fluid (CSF) compartment. Temperature gradients of the CSF may in turn influence the temperature of brain parenchyma (1) directly, along the extensive contact area between the cerebrocortical surface and the CSF-compartment, or (2) indirectly, via brain arteries that extend over long distances and arborize within the subarachnoid space before entering the pial vascular network and brain parenchyma. Numerous subarachnoid and pial arterial branches exposed to the CSF have diameters in the range of the vessels of the retia mirabilia of animals in which selective brain cooling has been clearly established experimentally. It is also shown that the arrangements of venous plexuses within the vertebral canal provide anatomical preconditions for a cooling of the spinal cord via the CSF. The possibility of spinal cord and spinal ganglia cooling by temperature convection via venous blood — cooled in the venous networks of the skin of the backflowing through numerous anastomoses to the external and internal vertebral plexuses and, finally, into the vascular bed of the spinal dura is discussed on the basis of anatomical facts.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Alcolado R, Weller RO, Parrish EP, Garrod D (1988) The cranial arachnoid and pia mater in man: anatomical and ultrastructural observations. Neuropathol Appl Neurobiol 14:1–17

    Google Scholar 

  • Amenta F, Snacesario G, Ferrante F, Cavallotti C (1980) Acetyl- cholinesterase-containing nerve fibers in the dura mater of guinea pig, mouse and rat. J Neural Transm 47:237–242

    Google Scholar 

  • Andres KH (1967) Über die Feinstruktur der Arachnoidea und Dura mater von Mammalia. Z Zellforsch 79:272–295

    Google Scholar 

  • Andres KH, Duering MV, Muszynski K, Schmidt RF (1987) Nerve fibers and their terminals of the dura mater encephali of the rat. Anat Embryol 175:289–301

    Google Scholar 

  • Baker MA (1979) A brain cooling system in mammals. Sci Am 240:114–122

    Google Scholar 

  • Baker MA (1982) Brain cooling in endotherms in heat and exercise. Annu Rev Physiol 44:85–96

    Google Scholar 

  • Batson OV (1957) The vertebral vein system. Am J Roentgenol 78:195–212

    Google Scholar 

  • Brengelmann GL (1987) Dilemma of body temperature measurement. In: Shiraki K, Yousef MK (eds) Man in stressful environments, thermal and work physiology. Thomas, Springfield, Ill, pp 5–22

    Google Scholar 

  • Brinnel H, Cabanac M, Hales JRS (1987) Critical upper level of body temperature, tissue thermosensitivity and selective brain cooling in hyperthermia. In: Hales JRS, Richards DAB (eds) Heat stress, physical exertion and environment. Elsevier, Amsterdam, pp 209–240

    Google Scholar 

  • Butler AB, Douglas Mann J, Maffeo CH, Dacey RG, Jr, Johnson RN, Bass NH (1983) Mechanisms of cerebrospinal fluid absorption in normal and pathologically altered arachnoid villi. In: Wood JH (ed) Neurobiol cerebrospinal fluid. Plenum Press, New York London

    Google Scholar 

  • Cabanac M (1993) Selective brain cooling in humans: “fancy” or fact? FASEB J 7:1143–1146

    Google Scholar 

  • Cabanac M, Brinnel H (1985) Blood-flow in the emissary veins of the human head during hyperthermia. Eur J Appl Physiol 54:172–176

    Google Scholar 

  • Caputa M, Perrin G, Cabanac M (1978) Ecoulement sanguin reversible dans la veine ophthalmique: mécanisme de refroidissement sélectif du cerveau humain. C R Acad Sci 87D: 1011–1014

    Google Scholar 

  • Cloyd MW, Low FN (1974) Scanning electron microscopy of the subarachnoid space in the dog. I. Spinal cord levels. J Comp Neurol 153:325–368

    Google Scholar 

  • Deklunder G, Dauzat M, Lecroart JL, Hauser JJ, Houdas Y (1991) Influence of ventilation of the face on thermoregulation in man during hyper- and hypothermia. Eur J Appl Physiol 62: 342–348

    Google Scholar 

  • Dijk DJ, Landolt HP, Moser S, Wieser HG, Borbély AA (1994) Brain temperature recorded at the parahippocampal gyrus exhibits a 24-h rhythm in humans abstract. Eurosleep '94. 12th Congress of the European Sleep Research Society, Firenze, 22–27 May

  • Dimitridaou V, Buzzi MG, Moskowitz MA, Theoharides TC (1991) Trigeminal sensory fiber stimulation induces morphological changes reflecting secretion in rat dura mater mast cells. Neuroscience 44:97–112

    Google Scholar 

  • Düring VM, Bauersachs M, Böhmer B, Veh RW, Andres KH (1990) Neuropeptide Y- and substance P-like immunoreactive nerve fibers in the rat dura mater encephali. Anat Embryol 182:363–373

    Google Scholar 

  • Edvinsson L, Uddman R (1981) Adrenergic, cholinergic and peptidergic nerve fibers in dura mater — involvement in headache? Cephalalgia 1:175–179

    Google Scholar 

  • Edvinsson L, Emson P, McCulloch J, Tatemotot K, Uddman R (1983) Neuropeptide Y: cerebrovascular innervation and vasomotor effects in the cat. Neurosci Lett 43:79–84

    Google Scholar 

  • Edvinsson L, Brodin E, Jansen I, Uddman R (1988) Neurokinin A in cerebral vessels: characterization, localization and effects in vitro. Regul Pept 20:181–197

    Google Scholar 

  • Elias H, Schwartz D (1971) Cerebrocortical surface areas, volumes, lengths of gyri and their interdependence in mammals, including man. Z Saeugetierkd 36:147–163

    Google Scholar 

  • Faraci FM, Kadel KA, Heistad DD (1989) Vascular responses of dura mater. Am J Physiol 257:H157-H161

    Google Scholar 

  • Furness JB, Papka RE, Della NG, Costa M, Eskay RL (1982) Substance P-like immunoreactivity in nerves associated with the vascular system of guinea-pigs. Neuroscience 7:447–459

    Google Scholar 

  • Gisel A (1958) Ueber die Emissaria parietalia et mastoidea des menschlichen Schädels. Hyrtl-Almanach I:73–122

    Google Scholar 

  • Haines DE, Frederickson RG (1991) The meninges. In: Al-Mefty O (ed) Meningiomas. Raven Press, New York, pp 9–24

    Google Scholar 

  • Haines DE (1991) On the question of a subdural space. Anat Rec 230:3–21

    Google Scholar 

  • Hayward JN, Baker MA (1969) A comparative study of the role of the cerebral arterial blood in the regulation of brain temperature in five mammals. Brain Res 16:417–440

    Google Scholar 

  • Hirashita M, Shido O, Tanabe M (1992) Blood flow through the ophthalmic veins during exercise in humans. Eur J Appl Physiol 64:92–97

    Google Scholar 

  • Jessen C, Kuhnen G (1992) No evidence for brain stem cooling during face fanning in humans. J Appl Physiol 72:664–669

    Google Scholar 

  • Keller JT, Marfurt CF (1991) Peptidergic and serotoninergic innervation of the rat dura mater. J Comp Neurol 309:515–534

    Google Scholar 

  • Kerber CW, Newton TH (1973) The macro and microvasculature of the dura mater. Neuroradiology 6:175–179

    Google Scholar 

  • Klika E (1967) The ultrastructure of meninges in vertebrates. Acta Univ Carol [Med] (Praha) 13:53–71

    Google Scholar 

  • Knyihar-Scillik E, Tajti J, Mohtasham S, Sari G, Vecsei L (1995) Electrical stimulation of the Gasserian ganglion induces structural alterations of calcitonin gene-related peptide-immunoreactive perivascular sensory nerve terminals in the rat cerebral dura mater: a possible model of migraine headache. Neurosci Lett 184:189–192

    Google Scholar 

  • Krahn V (1982) The pia mater at the site of the entry of blood vessels into the central nervous system. Anat Embryol 164: 257–263

    Google Scholar 

  • Krisch B (1988) Ultrastructure of the meninges at the site of penetration of veins through the dura mater, with particular reference to Pacchionian granulations. Cell Tissue Res 251:621–631

    Google Scholar 

  • Krisch B, Leonhardt H, Oksche A (1983) The meningeal compartments of the median eminence and the cortex. Cell Tissue Res 228:597–640

    Google Scholar 

  • Krisch B, Leonhardt H, Oksche A (1984) Compartments and perivascular arrangement of the meninges covering the cerebral cortex of the rat. Cell Tissue Res 238:459–474

    Google Scholar 

  • Kuhnen G, Jessen C (1994) Thermal signals in control of selective brain cooling. Am J Physiol 267 R:355–359

    Google Scholar 

  • Landolt HP, Moser S, Wiesen HG, Borbeley AA, Dijk DJ (1995) Intracranial temperature across 24 hour sleep wake cycles in humans. Neuroreport 6:913–917

    Google Scholar 

  • Mayberg M, Zervas NT, Moskowitz MA (1984) Trigeminal projections to supratentorial, pial and dural blood vessels in cats demonstrated by horseradish peroxidase histochemistry. J Comp Neurol 233:46–56

    Google Scholar 

  • Nabeshima S, Reese TS, Laudis DMD, Brightman MW (1975) Junctions in the meninges and marginal glia. J Comp Neurol 164:127–170

    Google Scholar 

  • Nielson B (1988) Natural cooling of the brain during outdoor bicycling? Pflügers Arch 411:456–461

    Google Scholar 

  • Numely SA, Nelson DA (1992) Human head cooling: mechanism and modeling. In: Lotens WA, Havenith G (eds) Proceedings of the Fifth International Conference on Environmental Ergonomics. TNO Inst Soesterburg, The Netherlands, p 134

    Google Scholar 

  • Orlin JR, Osen KK, Hovig T (1991) Subdural compartment in pig: a morphologic study with blood and horseradish perioxidase infused subdurally. Anat Rec 230:22–37

    Google Scholar 

  • Roland J, Bernard C, Bracard S, Czorny A, Floquet J, Race JM, Forlodou P, Picard L (1987) Microvascularization of the intracranial dura mater. Surg Radiol Anat 9:43–49

    Google Scholar 

  • Schachenmayr W, Friede RL (1978) The origin of subdural neomembranes. Am J Pathol 92:53–62

    Google Scholar 

  • Silverman J, Kruger L (1989) Calcitonin-gene-related-peptide immunoreactive innervation of the rat head with emphasis on specialized sensory structures. J Comp Neurol 280:303–330

    Google Scholar 

  • Simoens P, Lauwers H, De Geest JP, De Schaepdrijver L (1987) Functional morphology of the cranial retia mirabilia in the domestic mammals. Schweiz Arch Tierheilkd 129:295–307

    Google Scholar 

  • Steinmann WF (1984) Makroskopische Präparationsmethoden in der Medizin. Thieme, Stuttgart

    Google Scholar 

  • Stöhr PJ (1928) Die peripherischen Anteile des vegetativen Nervensystems. Handbuch der mikroskopischen Anatomie des Menschen, vol 4. Springer, Berlin, pp 265–447

    Google Scholar 

  • Suzuki N, Hardebo JE, Owman C (1988) Origin and pathways of cerebrovascular vasoactive intestinal polypeptide-positive nerves in rat. J Cereb Blood Flow Metab 8:697–712

    Google Scholar 

  • Suzuki N, Hardebo JE, Owman C (1989) Origins and pathways of cerebrovascular nerves storing substance P and calcitonin gene-related peptide in rat. Neuroscience 2:427–438

    Google Scholar 

  • Wenger CB (1987) More comments on “Keeping a cool head”. News Pharamcol Sci 2:150

    Google Scholar 

  • Whitby JD, Dunkin LJ (1971) Cerebral, oesophageal and nasopharyngeal temperatures. Br J Anaesth 43:673–676

    Google Scholar 

  • Zenker W, Rinne B, Bankoul S, Le Hir M, Kaissling B (1992) 5′-Nucleotidase in spinal meningeal compartments in the rat — an immuno- and enzyme histochemical study. Histochemistry 98:135–139

    Google Scholar 

  • Zenker W, Bankoul S, Braun JS (1994) Morphological indications for considerable diffuse reabsorption of cerebrospinal fluid in spinal meninges particularly in the areas of meningeal funnels. An electronmicroscopical study including tracing experiments in rats. Anat Embryol 189:243–258

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zenker, W., Kubik, S. Brain cooling in humans — anatomical considerations. Anat Embryol 193, 1–13 (1996). https://doi.org/10.1007/BF00186829

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00186829

Key words

Navigation