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Acta Otolaryngol 2001; 121: 839 – 843 Arterial Blood Supply to the Auditory Cortex of the Chinchilla JASWINDER PANESAR, HORMOZ HAMRAHI, NOAM HAREL, NAOKI MORI, RICHARD J. MOUNT and ROBERT V. HARRISON From the Auditory Science Laboratory, Department of Otolaryngolog y, Uni×ersity of Toronto, Brain & Beha×iour Di×ision, The Hospital for Sick Children, Toronto, Ont., Canada Panesar J, Hamrahi H, Harel N, Mori N, Mount RJ, Harrison RV. Arterial blood supply to the auditory cortex of the chinchilla. Acta Otolaryngol 2001; 121: 829 – 843. Utilizing optical imaging we identi ed and named the arteries that supply the primary auditory cortex in the chinchilla (Chinchilla laniger). The primary auditory cortex is located 2 – 3 mm caudal to the medial cerebral artery and is supplied by it. Using corrosion casts and scanning electron microscopy we visualized the capillary networks in the auditory cortex and found regional variations in the densities of the capillary bed. We hypothesize that the uneven capillary densities observed in the auditory cortex correspond to neurologically more active areas. Key words : capillary network, corrosion cast, medial cerebral artery, optical imaging, primary auditory cortex. INTRODUCTION The relationship between neural activity in the cerebral cortex and local hemodynamics has become a topic of considerable interest and importance since the introduction and wide-scale use of clinical imaging methods such as positron emission tomography and functional magnetic resonance imaging (fMRI) (1 – 3). These techniques, together with optical imaging of intrinsic signals (4, 5), are all techniques in which the signal detected is a hemodynamic event, often referred to as a blood oxygen level- dependent (BOLD) effect. In our experimental work, using optical imaging of intrinsic signals in the auditory cortex, we have used a chinchilla (Chinchilla laniger) animal model (6, 7). However, to date there has been no systematic study of the arterial blood supply to auditory areas of the cortex in the chinchilla (or in similar small rodents). The chinchilla has been widely used as a model to study the function of the auditory system, particularly in North America where it is widely available. This species has a number of advantages for hearing research: it can be trained in behavioral psychophysical tasks, and anatomically it has an accessible inner ear via an enlarged middle ear bulla cavity. For auditory cortical recordings, the cranium and dura overlying the temporal cerebrum can be safely removed (8). There are three components to the present study. Firstly, we have determined the exact location of the auditory cortex using optical imaging of intrinsic signals and determined as far as possible the relationship between primary auditory cortex and local blood vessels. Secondly, we have used latex polymer infusion techniques to ll and mark the arterial blood supply to the brain. From such whole brain preparations we describe and provide nomenclature for the © 2001 Taylor & Francis. ISSN 0001-648 9 major arterial vessels to the auditory cortex. Thirdly, we have used corrosion cast techniques combined with scanning electron microscopy (SEM) to visualize the artery– arteriole connections which supply capillary networks in the auditory cortex. MATERIALS AND METHODS Adult chinchillas (n¾ 11; weight 500 – 750 g) were studied. All invasive procedures were carried out in anesthetized animals using ketamine hydrochloride (15 mg kg, i.m.), atropine sulphate (0.04 mg kg, i.m.) and xylazine hydrochloride (2.4 mg kg, i.m.). All methods conformed strictly to the guidelines of the Canadian Council on Animal Care. In three subjects, optical imaging of intrinsic signals was carried out to determine the boundaries of the auditory cortex. We have previously described these methods in detail (6, 7). Brie y, via a 10-mm wide craniotomy over the temporal lobe, optical images of the cortex were recorded during acoustic stimulation (broadband noise, 80 dB SPL). Using suitable monochromatic illumination (wavelength : 540 – 560 nm), local hemodynamic changes in response to the metabolic demands of active auditory neurons were imaged with a suitable detection system. The derived functional maps, i.e. boundary of active auditory cortex, and images of the super cial vasculature were then compared. A second group of animals (n ¾5) were used for whole brain blood vessel identi cation studies. Using a trans-cardiac cannulation technique, subjects were perfused with : 1000 ml of heparinized saline. The descending aorta was then clamped and the ascending aorta infused with latex. Return of ow was achieved by incising the right atrium. Approximatel y 15 – 20 ml of latex was used to ensure complete lling of all major cerebral arteries and their branches. 840 J. Panesar et al. For high resolution microscopy of arterial connections to capillary beds a corrosion casting technique (9) was employed in a third group of animals (n ¾3). Casts of the cerebral vasculature were prepared by perfusing, again via the ascending aorta, 50 ml of heparinized PBS followed by 20 ml of Batson’s 17 resin. Complete polymerization of the resin took : 12 h, after which the brain was dissected from the cranium. Soft tissue was macerated in 40% KOH at 50°C for 24 h with intermittent distilled water rinses. The plastic cast was air-dried, mounted onto a stub with colloidal silver and sputter-coated. RESULTS AND DISCUSSION Position of auditory cortex Optical imaging of intrinsic signals essentially shows areas of increased blood ow that are directly related to metabolic demands of activity in the auditory cortex resulting from acoustic stimulation. Fig. 1 shows results from three typical subjects. Each panel shows an image of temporal cortex through the craniotomy, with the boundary of the auditory areas superimposed (black lines). Generally it is possible to recognize three separate areas of hemodynamic change, which we identify as primary auditory cortex (AI), secondary auditory cortex (AII) and the anterior auditory eld (AAF). The position of the AI as identi ed by optical imaging corresponds to the electrophysiologically de ned AI in the chinchilla (8). Single-unit recordings from the area have short onset latency responses that are characteristic of primary auditory neurons (7). As a rule of thumb we can say that the AI is situated 2 – 3 mm posterior (caudal) to the medial cerebral artery (MCA) along the middle temporal artery (MTA). Often the AI coincides with the bifurcation of the MTA into its superior and inferior branches, but as the location of the bifurcation varies somewhat this is not always the case. Major arterial ×essels Intra-aortic latex infusion allows reliable visualiza- Acta Otolaryngol 121 tion of all major cerebral arteries, as shown in Fig. 2. Viewed from the ventral direction (lower panel), the anatomy of the arterial circle and its associated major vessels can be seen. The general plan (from caudal to rostral) of vertebral arteries converging to form the basilar artery, which in turn bifurcates to form the caudal end of the arterial circle, is similar in all mammalian species, including humans. The arterial circle of the chinchilla resembles that of other rodents (10) and is analogous to the circle of Willis in primates (11). The cerebellum is supplied by the caudal and rostral cerebellar arteries. The caudal cerebellar artery arises from the basilar artery at the lower part of the pons whilst the rostral cerebellar artery arises at the termination of the basilar artery, close to the upper border of the pons. The arterial supply of the cerebral cortex is provided by the three cerebral arteries: caudal, medial and rostral. The caudal cerebral arteries are given off at the cerebral peduncle. Each caudal cerebral artery is joined to the internal carotid artery by the caudal communicating artery. The relative diameter of the internal carotid arteries of the chinchilla, and presumably of rodents in general, is considerably reduced compared to those in humans. Of particular interest here is the MCA, which supplies most of the temporal cortex including all auditory areas. It courses laterally along the sulcus between the frontal and temporal lobes. The medial cerebral and rostral cerebral arteries are given off anterior to the internal carotid arteries. The rostral cerebral artery runs medially to reach the longitudinal ssure between the two cerebral hemispheres above the optic chiasm. In many mammalian species the rostral cerebrals are joined by the rostral communicating artery; however, in seven of the eight chinchillas examined this communicating artery was lacking, and thus the arterial circle is not fully closed. Similarly, Jablonski and Brudnicki (12) noted rostral communicating arteries in only 2 of 28 chinchillas examined. Fig. 1. Optical imaging of intrinsic signal results from three typical subjects, in response to acoustic stimulation. Acta Otolaryngol 121 Arterial blood supply to auditory cortex of the chinchilla 841 Fig. 2. Chinchilla brain following aortic latex infusion showing all major cerebral arteries. The upper image in Fig. 2 is a lateral view of the chinchilla brain showing the MCA and its branches. The MCA, coursing laterally around the surface of the temporal cerebrum, gives rise to three main arteries supplying the temporal lobe: the inferior, middle and superior temporal arteries. The MTA (our particular focus here) further divides into superior and inferior branches. Fig. 3 is a schematic representation summarizing the major arterial supply associated with the auditory cortex. Whilst variations in the arterial tree may be expected and comparative studies by Jablonski and Brudnicki (12) have demonstrate d variations in the caudal cerebral arteries, the location of the branch point of the MCA and MTA is remarkably consistent. In making a craniotomy for electrophysiological Fig. 3. A schematic representation summarizing the major arterial supply associated with the auditory cortex (not to scale). 842 J. Panesar et al. Acta Otolaryngol 121 or optical studies of the auditory cortex we can recommend using the following surgical landmarks. Anteriorly (rostrally), the caudal wall of the orbit overlies the MCA; using the zygoma as a ventral boundary and the horizontal part of the parietofrontal bone as the dorsal edge, a craniotomy will reveal temporal cortex with the MTA running centrally across it. Final connections to cortical capillary network The nal stages in the supply of blood to the auditory cortex are depicted in Fig. 4. Fig. 4a is an SEM image of the corrosion cast of vasculature viewed from the caudal direction looking along the cortical surface at the bifurcation of the MTA into superior (sMTA) and inferior (iMTA) branches. The lower surfaces of both the inferior and superior branches of the MTA give rise to collateral vessels which directly penetrate the cortical surface. In addition there are a number of side-branching collateral vessels which tend to either extend from the artery at right-angles across the cortical surface for a short distance ( : 500 mm) before penetrating the surface, or have a super cial course of several millimeters before becoming intracortical. Some arteries give rise to a capillary bed : 750 mm deep located in the super cial layer of the cortex. Other arteries contribute few if any collateral branches to this capillary bed, penetrating deeply into the cortex. Some of the latter type bend at 90° and course parallel to the cortical surface at a depth of : 1 mm and give rise to upward-coursing arterioles which contribute to the overlying capillary bed. Within the super cial capillary bed, arterioles give off both collateral and terminal capillaries. The super cial capillary bed is not evenly distributed throughout the temporal cortex. It is shown in Fig. 4a and c that there are areas of dense capillary networks separated by regions of few to no capillaries. It is our working hypothesis that the uneven capillary bed densities that we observe in auditory areas of temporal cortex may correspond to regions in which auditory neurons are more active, or perhaps more densely packed, demanding differing amounts of hemoglobin supply. Fig. 4. Fig. 4. SEM images of corrosion cast of cerebral vasculature supplying the auditory cortex. (a) View from the caudal direction looking along the cortical surface at the bifurcation of the MTA into sMTA and iMTA branches. (b) An arteriole bifurcates with one branch (½ ) giving rise to the super cial capillary network and the other (*) penetrating deeper into the cortex without further branching. (c) Two dense regions of the super cial capillary network are separated by a low density region which is penetrated by an intracortical arteriole (*). Arterial blood supply to auditory cortex of the chinchilla Acta Otolaryngol 121 ACKNOWLEDGMENTS This research was supported by grants from the Medical Research Council (Canada) and by the Masonic Foundation of Ontario. 8. 9. REFERENCES 1. Ogawa S, Tank DW, Menon R, et al. Intrinsic signal changes accompanying sensory stimulation: functional brain mapping with magnetic resonance imaging. Proc Natl Acad Sci USA 1992; 89: 5951– 5. 2. Kwong KK, Belliveau JW, Chesler DA, et al. Dynamic magnetic resonance imaging of human brain activity during primary sensory stimulation. Proc Natl Acad Sci USA 1992; 89: 5675 –9. 3. Fox PT, Raichle ME. Focal physiological uncoupling of cerebral blood ow and oxidative metabolism during somatosensory stimulation in human subjects. Proc Natl Acad Sci USA 1986; 83: 1140– 4. 4. Bonhoeffer T, Grinvald A. Iso-orientation domains in cat visual cortex are arranged in pinwheel-like patterns. Nature 1991; 353: 429 – 31. 5. Grinvald A, Leike E, Frostig RD, Gilbert CD, Wiesel TN. Functional architecture of cortex revealed by optical imaging of intrinsic signals. Nature 1986; 324: 361 – 4. 6. Harrison RV, Harel N, Kakigi A, Raveh E, Mount RJ. Optical imaging of intrinsic signals in chinchilla auditory cortex. Audiol Neurootol 1998; 3: 214 –23. 7. Harel N, Mori N, Sawada S, Mount RJ, Harrison RV. Three distinct auditory areas of cortex (AI, AII, AAF) . 10. 11. 12. 843 de ned by optical imaging of intrinsic signals. Neuroimage 2000; 11: 302– 12. Harrison RV, Kakigi A, Hirakawa H, Harel N, Mount RJ. Tonotopic mapping in auditory cortex of the chinchilla. Hear Res 1996; 100: 157– 63. Murakami T. Application of the scanning electron microscope to the study of the ne distribution of the blood vessels. Arch Histol Jpn 1971; 32: 445– 54. Popesko P, Rajtova V, Horak J. Colour atlas of the anatomy of small laboratory animals, Vols. 1, 2. London: Wolfe Publishing Ltd, 1992. Williams PL, ed. Gray’s anatomy. The anatomical basis of medicine and surgery. New York: Churchill Livingstone, 1995. Jablonski R, Brudnicki W. The effect of blood distribution to the brain on the structure and variability of the cerebral arterial circle in musk-rat and in chinchilla. Folia Morphol (Warsz) 1984; XLIII: 109– 14. Submitted March 17, 2000; accepted April 26, 2001 Address for correspondence: Dr. Robert V. Harrison Auditory Science Laboratory Dept. of Otolaryngology The Hospital for Sick Children 555 University Avenue Toronto, Ont. M5G 1X8 Canada Tel.: »1 416 813 6535 Fax: » 1 416 813 8456 E-mail: [email protected]