(Hypertension. 1997;30:693.)
© 1997 American Heart Association, Inc.
Articles |
A Descriptive and Quantitative Light and Electron Microscopy Study of the Aortic Depressor Nerve in Normotensive Rats
From the Department of Biological Sciences, School of Medicine of Triângulo Mineiro, Uberaba, Minas Gerais (V.P.S.F.), and the Departments of Physiology (H.C.S.) and Neurology (A.A.B.) and University Hospital, School of Medicine of Ribeirão Preto, USP, Ribeirão Preto, São Paulo, Brazil.
Correspondence to Dr. A.A. Barreira, Departamento de Neurologia, Faculdade de Medicina de Ribeirão Preto (USP), A. Bandeirantes 3 900, 14 049-900, Ribeirão Preto, SP, Brazil.
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Abstract |
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Abstract There is no literature report of a detailed morphologic study of the aortic depressor nerve. The aim of this study was to describe the general morphological aspects and to obtain morphometric parameters for the aortic depressor nerve of normotensive Wistar rats (n=12). Before the morphologic studies, nerves were isolated and pressure-nerve activity curves were obtained. Basal mean arterial pressure was 117±5 mm Hg, the systolic pressure threshold was 100±7 mm Hg, and mean arterial pressure at 50% of maximal activity was 115±5 mm Hg and the baroreceptor gain 1.99±0.09%/mm Hg. Semithin and thin sections of proximal and distal nerve segments were then examined by light and electron microscopy, respectively. The main nerve components were (1) unmyelinated and myelinated axons; (2) Schwann cells; (3) capillary wall endothelial cells and pericytes; (4) collagen fibers in the epineurium and endoneurium and between perineurial cell layers; and (5) fibroblasts and mast cells. The depressor nerves were found to contain 204-996 axons per nerve, 80% of which, on average, were unmyelinated, with a 4:1 unmyelinated/myelinated axon ratio. The unmyelinated axon histogram was unimodal, with a mean diameter of 0.5±0.02 µm. Myelinated fibers had axons averaging 1.3±0.06 µm in diameter and representing 53% of the total fiber diameter. The ratio between axonal and total fiber diameter of myelinated fiber ranged from 0.4 to 0.8 and tended to increase with axon size. Proximal and distal segments were morphologically similar. In conclusion, the morphologic description of the depressor nerve provides important data for further investigations of the structural basis of altered baroreflex responses in conditions such as arterial hypertension, aging, atherosclerosis, and peripheral neuropathies.
Key Words: rat peripheral nervous system • aortic depressor nerve • peripheral nerves • nerve morphology • normal nerves
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Introduction |
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The aortic mechanoreceptors are a nerve arborization located in the adventitia of the ascending aorta whose endings are the origin of myelinated (fast conducting) and unmyelinated (slow conducting) afferent nerve fibers. In mammalian species commonly used in laboratories, aortic nerve fibers (Cyon nerve) travel to the central nervous system either along the main vagus trunk or along a slender nerve, the aortic or depressor nerve.1 In the rat, the depressor nerves have been found to arise from the aorta on the left side and the subclavian and innominate arteries on the right side. A third route has been described, with fibers passing through the recurrent laryngeal nerve, the communicating branch, and the superior laryngeal nerve into the vagus.2 The left aortic depressor nerve can be easily identified in about 50% of the rats and the right one is less regularly present as a separate strand.3 Krieger and Marseillan1 have described certain aspects of the course and branches of the depressor nerve of rats, but information on the composition of the nerve has come mainly from studies on cats.4 The depressor nerve of the rat has not been studied as extensively as that of the cat, despite the considerable attention that has been given to the rat aortic baroreceptors.
The electrophysiological characteristics of rat aortic baroreceptor discharge involving myelinated and unmyelinated afferent fibers of the depressor nerve have been well explored.5 6 7 The relationship between aortic wall and baroreceptor properties and their relationship with connective tissue have been well established.8 Although the sensory terminals of the depressor nerve and aortic baroreceptors have been studied by several investigators at the light9 and electron microscopic10 levels, a detailed morphologic study of the aortic depressor nerve has not been reported. Therefore, the objectives of the present study were to investigate the general morphological aspects of the aortic depressor nerve of rats and to determine their morphometric parameters, including the number and size of myelinated and unmyelinated fibers. The electrophysiological characteristics of all nerves were determined before the morphologic analysis.
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Methods |
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Experiments were performed on 12 normotensive male Wistar rats (250 to 400 g). The animals were anesthetized with sodium pentobarbital (Nembutal, 40 mg/kg, IP). The left aortic depressor nerve, when present as a separate strand, was carefully isolated for recording baroreceptor activity, and the right carotid artery was cannulated for pressure measurement and the right femoral artery for blood withdrawal and reinfusion. The methods used to obtain the pressure-nerve activity curve were described in detail elsewhere.11 12 13 Briefly, the nerve activity was amplified using a differential high impedance preamplifier (model 113, Princeton Applied Research) and the signal was passed through a customized band-pass active filter (100 Hz to 3 kHz). Nerve activity was displayed on an oscilloscope (model 5113, Tektronics, Inc) and monitored over a loudspeaker. A nerve traffic analyzer (model 605C, University of Iowa Bioengineering) was used to count action potentials that exceeded a selected voltage immediately above the noise level.
The output from the spike counter was in spikes per second (rate mode) with a time constant of 200 ms. This activity was digitally recorded by an analog to digital interface (Lynks, Tecnologia Eletrônica ltda) and recorded (100 Hz) in a personal computer (IBM/PC-AT 486) simultaneously with the pulsatile carotid pressure.
To assess baroreceptor firing range, rats were submitted to rapid changes (20 to 30 seconds) in arterial pressure by withdrawal and reinfusion of blood. The systolic pressure threshold (SPth), E, minimum systolic pressure that triggers baroreceptor activity, and the pressure-nerve activity curve were determined. The mean arterial pressure at 50% of maximal activity (MAP50) and the baroreceptor gain were calculated from the pressure-nerve activity curve by means of a nonlinear regression based on Levemberg-Marquadt algorithm called logistic sigmoidal regression.
After the electroneurographic recordings, the proximal segment of the nerves was repaired and approximately 1.5 to 2.0 cm was removed and fixed overnight in 2.5% glutaraldehyde. Proximal (close to nodose ganglion) and distal (at clavicular level) segments were post-fixed in 1% OsO4 solution for two hours at 4°C, dehydrated with graded ethanol, rinsed in a propylene oxide solution, and embedded in epoxy resin (Polibed 812). The nerves were oriented to permit semithin (0.2 to 0.3 µm) transverse sections of the fascicles, which were stained with 1% toluidine blue and examined by light microscopy. A photomicrograph of the whole nerve transverse section at 320x magnification was obtained under the oil immersion lens with an Axiophot photomicroscope (Carl Zeiss) and magnified to 3200x. The perineurium cell layers and the capillary vessels were identified by visual inspection and counted. The luminal diameters of capillaries present inside the fascicles were measured with an image analysis system (Mini-Mop, Kontron Byldanalise) and the total number of myelinated fibers was counted. The area and diameter were measured for each fascicle (excluding the perineurium) and for each myelinated fiber visible on the photomicrographs. For each nerve with two fascicles, we obtained the total fascicular area by summing the areas of the two individual fascicles. Hereafter, the term fascicular area will be used as a synonym of total fascicular area. The percentage of the total fascicular area occupied by the myelinated fibers and the myelinated fiber density were calculated. In the case of myelinated axons, both axonal diameter (defined by the outer limit of the axolemma) and fiber diameter (defined by the outer limit of the myelin lamellae) were measured and the ratio between the two diameters was obtained. This ratio is designated g.14 The unmyelinated fibers were studied with a transmission electron microscope (Phillips EM 208). Thin sections (500 to 600 nm) were mounted on 200-mesh Athene grids and stained with lead citrate and uranyl acetate. At least five electron micrographs at 3000x original magnification were obtained at random for each nerve without superposition of microscopic fields and magnified to 15,000x. With the Mini-Mop analysis system, the unmyelinated fibers visible on the electron micrographs were counted and their area and diameter were measured. The percentage of the total fascicular area occupied by these fibers and their density were also calculated. The number of unmyelinated axons associated with each Schwann cell or portion thereof (hereafter called a Schwann cell unit) was determined in six depressor nerves using the basal lamina to outline the limits of a given Schwann cell unit. The term Schwann cell body is used for the portion of the cell containing the nucleus.15 The number of Schwann cell nuclei present in each transverse section of the depressor nerve was counted and their density calculated. Histograms of the frequency distribution of the myelinated and unmyelinated fibers were constructed and separated into class intervals increasing by 0.5 and 0.1 µm, respectively.
Significant differences between mean values (mean±SD or mean±SEM) of proximal and distal segments were determined by paired Student’s t test and a level of significance of P<.05 was adopted. Pearson correlation coefficients (r2) and slopes were calculated using equations for simple linear correlation and regression.
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Results |
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Physiological Studies
The pressure-nerve activity curves indicate that the animals from which the nerves were studied presented basal mean arterial pressure of 117±5 mm Hg, systolic threshold pressure of 100±7 mm Hg, mean arterial pressure at 50% of maximal activity of 115±5 mm Hg, and the baroreceptor gain of 1.99±0.09% (Fig 1).
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Morphological Aspects
In 83% of cases (10 of 12) the aortic depressor nerve
consisted of a single fascicle and, in the other cases, two separate
nerves were present and identified only at the proximal nerve
level. The epineurium of the depressor nerves was found to consist of
connective tissue with largely longitudinally collagen fibers, larger
than those found in the endoneurium and the perineurium, and blood
vessels. All depressor nerve fascicles were delimited by three or four
thin, closely apposed layers of flattened cells, with a prominent basal
lamina, between which lay longitudinally oriented collagen fibers that
constituted the perineurium (Fig 2). The
endoneurium consisted mainly of longitudinally oriented collagen fibers
that occupied much of the space between the myelinated and
unmyelinated axons (Fig 2). An obvious clustering of
unmyelinated axons, localized peripherally
within the endoneurium, was evident in 66.7% (8 of 12) of nerves and
was observed only in the distal segment (Fig 2). There was no regional
separation of myelinated and unmyelinated axons
in the proximal segments of the nerve. Only half (6 of 12) of the
depressor nerves presented a single capillary vessel within the
endoneurium. In the two depressor nerves in which two separate
fascicles were present, only the larger one had a capillary. The
capillary wall consisted of endothelium, basal lamina
and pericytes (Fig 2). The other 6 nerves did not present any blood
vessel in their endoneurial space.
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The main components of the depressor nerve did not differ from those of the somatic nerves and were (1) unmyelinated and myelinated axons; (2) Schwann cells enveloping the axons; (3) capillary wall endothelial cells and pericytes; (4) connective tissue cells and collagen fibers in the endoneurium and between perineurial cells layers; and (5) fibroblasts and mast cells.
Morphometric Data
General Data
The fascicular area was 1.4±0.1 mm2
(range of 0.98 to 1.69) for the proximal segment and 1.6±0.1
mm2 (range of 0.98 to 2.49) for the distal segment. The
fascicular diameter was 36.9±1.6 µm (range of 25.2 to 44.1) for
the proximal segment and 36.9±2.1 µm (range of 29.6 to 54.6)
for the distal segment. The capillaries averaged 3.91±0.6 µm in
luminal diameter (ranges of 2.47 to 6.27 µm proximally and 2.24
to 5.04 µm distally).
Number and Size of Fibers
Depressor nerves contained on average 438 axons proximally (range
of 204 to 696, 19% of them myelinated and 81%
unmyelinated) and 492 axons distally (range of 238-996,
17% of them myelinated and 83% unmyelinated).
Nerve fibers were packed at a density of 332 axons per
mm2 of the fascicular area proximally (64±5
myelinated axons/mm2 and 260±41
unmyelinated axons/mm2) and 340 axons per
mm2 of the fascicular area distally (57±5
myelinated fibers/mm2 and 270±41
unmyelinated fibers/mm2). No significant
difference in total number of axons was found between the two segments
of the same nerve (P>.2 by paired t test).
Unmyelinated axons outnumbered myelinated axons
by a factor of four. Because small groups of fibers leave or enter the
depressor nerve along its cervical pathway,1 we assessed
the magnitude of the change in the number of axons along the length of
the nerve. Although it was evident that the number of axons was not
constant for proximal and distal segments of the depressor nerve, no
consistent pattern of change was detected. In four depressor
nerves examined (33.4%) there was no change from proximal to distal
segments in the number of myelinated axons. The range of
variability of myelinated axons from proximal to distal
fragments was -17.4% to 13.3%. The unmyelinated axons
presented a wider range of variability from proximal to distal
fragments (-64.9% to 40.4%), also with no consistent pattern
of change.
Most of the myelinated fibers in the depressor nerves examined were comparatively small, the total fiber diameter average being 2.4±0.1 µm proximally and 2.5±0.1 µm distally. The overall population of myelinated fibers had a unimodal size distribution which was skewed to the left (Fig 3). Approximately 97% of the myelinated fibers were less than 4 µm in total diameter and only about 16% of the fibers had a total diameter of 3 µm or greater. Myelinated fibers had axons that averaged 1.3±0.06 µm in diameter and constituted 53% of the total fiber diameter. The ratio of axon diameter to total fiber diameter (g) ranged from about 0.4 to 0.8 (mean value of 0.53±0.01) and tended to increase with increasing axon size (Fig 3). The correlation coefficient between axon diameter and g ranged from 0.36 to 0.85 in different nerves. Most nerves (9 in 12) presented correlation coefficients (r2) higher than 0.5.
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The mean diameters of unmyelinated axons was 0.5±0.07 µm proximally and 0.54±0.09 µm distally, with a unimodal distribution of size (Fig 4). Unmyelinated axons as small as 0.2 µm and as large as 1.4 µm were present in all nerves examined. About 55.5% of the proximal axons and 40.3% of the distal axons were less than 0.5 µm in diameter and 3.37% of the proximal axons and 4.46% of the distal ones were more than 1.0 µm in diameter. The distribution of sizes of unmyelinated axons showed considerable overlap with the corresponding distribution for myelinated axons and the largest unmyelinated axons (1.4 µm) were larger than 34.8% of the myelinated axons.
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Schwann Cells
An average of 87±8 Schwann cell units was found in each
nerve cross section. Each Schwann cell enveloped one to ten or more
unmyelinated axons (mean=2.97±1.5 axons/unit, n=519 units
in 6 nerves). No Schwann cell was devoid of axons. An average of
46.7±6.4% of the unmyelinated axons were not accompanied
by other axons in their Schwann cell envelopment. All axon sizes were
represented in this category, but the larger ones
predominated. When two or more axons were enveloped by the same Schwann
cell, the axons were not in contact with one another. Instead, each
axon was located in a separate Schwann cell trough (Fig 2). An average
of 20±5% of axons were enveloped in groups of two, and smaller
proportions of axons were enveloped in larger groups: three axons per
Schwann cell (8.8±3.5%), four axons (6.3±2.7%), five axons
(4.8±3.1%), and six to ten or more axons (4.2±2.8%). Axons of
different sizes were often enveloped by the same Schwann cell (Fig 2).
In each proximal or distal fascicular area there was an average of
12±1 Schwann cell nuclei (8±1 cell/mm2 of
nerve).
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Discussion |
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The physiologic characteristics of the depressor nerves studied are in agreement with those from our laboratory11 12 and from others.16 17 These parameters confirm that the morphologic features described are of typical aortic depressor nerves. All depressor nerves studied presented a defined perineurial envelopment, which consisted of three to four layers of perineurial cells. The lamellar arrangement of flattened cells separated by layers of collagenous connective tissue observed in the depressor nerve is the essential structural feature of the perineurium of peripheral mammalian nerves.18 The number of lamellae varies, mainly depending on the diameter of the fascicle: the larger the fascicle, the greater the number of lamellae.18 In the spinal nerves of rats, four layers could often be identified but a very small nerve was found to be covered by a single one.19 In all cases, the basal lamina was always present covering the outer and inner surfaces of the perineurial cells.18 19 Larger epineurial collagen fibers are a normal feature of other peripheral nerves of rats.19 20
Andresen et al,8 who studied transverse sections of six depressor nerves of Wistar-Kyoto rats, cut from the end closest to the aortic arch (distal segment) reported that the depressor nerve has 63 to 1379 unmyelinated axons and 20 to 86 myelinated axons. This result is quite different from ours, since the distal segments of the nerves studied here had 166 to 909 unmyelinated axons and 59 to 125 myelinated axons. This difference may be due to different methodologies used for preparing the nerve samples and counting the axons, to the smaller number of animals studied by Andresen et al, and to the different animal strains.
The total number of axons in the depressor nerve of other species has not been counted directly. In the cat, totals of 1200 to 2500 axons can be estimated from the number of myelinated axons known to be present if depressor nerves of cats also present an unmyelinated/myelinated axon ratio equal to 4:1. In two different light microscopy studies, the depressor nerves were obtained near the nodose ganglion. Devanandan4 reported that the depressor nerve of cats contains 243 to 251 myelinated fibers and Schmidt and Stromberg21 found an average of 542 myelinated axons (range of 386 to 836) in six swine nerves. We did not find any previous literature report about an electron microscopy analysis concerning the total number of fibers of the depressor nerve of any animal species.
The unmyelinated/myelinated fiber ratio obtained for the aortic depressor nerve of the rat (4:1) is closely similar to that of the human sural nerve,22 an afferent nerve whose morphology, morphometric parameters, and electrophysiology have been widely explored, and this is one of the morphologic characteristics that permit us to identify the aortic depressor nerve as an afferent nerve. The distribution of unmyelinated fiber diameter is constituted by one mode as it is for somatic and autonomic nerves. This distribution of the myelinated fibers of the depressor nerves of rats is unimodal instead of the bimodal distribution seen in somatic afferent nerves. In somatic nerves, different kinds of sensations travel along the fiber population of each mode. For example, in human sural nerves thin fibers (less than 7 µm in diameter) are responsible for nondiscriminative sensations (thermal and algesic sensations) and the larger ones (more than 7 µm) are responsible for discriminative sensations (vibration and position senses). Thus we may speculate that the unique depressor nerve fiber mode would be responsible for only one kind of function, ie, to conduct the afferent impulses of the baroreceptor reflex. From these data we can conclude that this nerve fiber distribution is very particular and can be comparable only to the carotid sinus nerve,15 another nerve conducting fast afferent impulses of an autonomic reflex.
The present study revealed that unmyelinated axons in the rat depressor nerve have average diameters of 0.39 to 0.59 µm proximally and 0.38 to 0.63 µm distally. These data are closely similar to those reported by Brown et al,5 who found unmyelinated axons with diameters of 0.25 to 0.9 µm in the depressor nerves of two rats. However, these authors studied a small number of nerves and did not show the distribution of these diameters, so that their data cannot be compared with ours.
Most of the myelinated axons in the depressor nerve are comparatively small. Devanandan4 reported that fibers 2-4 µm in diameter are most numerous in the cat. Schmidt and Stromberg21 found that myelinated fibers of the depressor nerve of swine are less than 10 µm in diameter and most of the A fibers in the 2-to 4- and 4- to 6-µm diameter range. In the rat, the average total fiber diameter is 2.4±0.1 µm proximally and 2.5±0.1 µm distally, and 97% of the fibers are smaller than 4 µm. This finding may be explained by the fact that rats are smaller animals than cats and swine, so that fibers having diameters of about 2 µm conduct at a velocity sufficient to elicit fast baroreflex responses in these animals.
Measurements of the conduction velocities of axons in the rat
depressor nerve indicated that unmyelinated axons (C
fibers) conduct at 0.5-2 m/s, the conduction velocity of thin
myelinated axons (A
and B fibers) ranges from 3 to 12
m/s, and the large myelinated axons conduct at 21.5-22.5
m/s.5 In the present study we did not measure the
conduction velocity of the depressor nerve but, using the scaling
factor of Gasser23 for calculating the conduction velocity
of unmyelinated axons in meters per second (1.7 times
axonal diameter) and that of Boyd and Kalu24 for computing
the corresponding value for small myelinated axons (4.6
times total fiber diameter), we may speculate that
unmyelinated axons in the rat depressor nerve conduct
action potentials at 0.3 to 2.4 m/s and the myelinated
axons conduct at 4.3 to 26.8 m/s. These estimates confirm the
physiological measurements of the conduction
velocity of the rat depressor nerve obtained by Brown et
al.5 Therefore, we speculate from these estimates that the
conduction velocities of unmyelinated and
myelinated fibers do not overlap despite the overlap in the
size ranges of the two types of axon.
The number of myelin layers and therefore the thickness of the myelin sheath are known to increase with increasing axonal diameter.25 26 The constancy of this relationship has been of considerable interest because of its relevance to the mechanism of saltatory conduction. Rushton14 found that when the ratio of axon diameter to total fiber diameter equals 0.6, which approximates average values observed in most nerves, the relationship is theoretically optimal for the spread of current from one node of Ranvier to the next. In the present study, myelinated fibers of the rat depressor nerve were found to have a mean g ratio equal to 0.53±0.01. Although g tended to increase over the range of axon diameters, there was considerable deviation in individual axons from a simple linear ratio. In fact, nerve fibers with identical axon diameters, but having myelin sheaths of different thickness, were frequently observed. This result is closely similar to those obtained for the rat sinus nerve20 and for the human sural nerve.21 Although the sinus nerve is a complex thoroughfare for axons of numerous functions and sources, the major axon component of this nerve is afferent (chemoreceptive and baroreceptive axons)15 and the author reported a mean g ratio equal to 0.64. The human sural nerve is the most common afferent nerve used in studies of peripheral neuropathies and presents a constant g ratio of 0.6.21
This is the first complete morphologic study of the aortic depressor nerve of rats. Because the rat is the most common model used in studies involving arterial pressure regulation, the detailed morphologic and morphometric description of the aortic depressor nerve associated with functional parameters provides important data for further investigation of the structural basis of altered baroreflex responses in conditions such as arterial hypertension, aging, atherosclerosis, and peripheral neuropathies.
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Acknowledgments |
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This study was supported by FAPESP and FAEPA. Valéria P.S. Fazan is the recipient of a fellowship from an Institutional Program for the Habilitation of Researchers (PICD), supported by CAPES. The authors thank Jaci A. Castania, Maria Cristina Lopes, and José A. Maulin for technical assistance.
Received March 17, 1997; first decision April 28, 1997; accepted May 13, 1997.
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References |
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TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. Krieger EM, Marseillan RF. Aortic depressor fibers in the rat: an electrophysiological study. Am J Physiol. 1963;205:771-774.
2. Andrew BL. A laryngeal pathway for aortic
baroreceptor impulses. J Physiol. 1954;125:352-360.
3. McCubbin JW, Masson MC, Page H. Aortic depressor nerves of the rat. Arch Intern Pharmacodyn. 1958;114:303-306.
4. Devanandan MS. A study of the
myelinated fibers of the aortic nerve of cats.
J Physiol. 1964;171:361-367.
5. Brown AM, Saum WR, Tuley FH. A comparison of
aortic baroreceptor discharge in normotensive and spontaneously
hypertensive rats. Circ Res. 1976;39:488-496.
6. Thorén P, Saum WR, Brown AM.
Characteristics of rat aortic baroreceptors with nonmedullary afferent
nerve fibers. Circ Res. 1977;40:231-237.
7. Brown AM, Saum WR, Yasui S. Baroreceptor
dynamics and their relationship to afferent fiber type and
hypertension. Circ Res. 1978;42:694-702.
8. Andresen MC, Krauhs JM, Brown AM. Relationship
of aortic wall and baroreceptor properties during development in
normotensive and spontaneously hypertensive rats. Circ
Res. 1978;43:728-738.
9. Aumonier FJ. Histological observations on the distribution of baroreceptors in the carotid and aortic regions of the rabbit, cat and dog. Acta Anat. 1972;82:1-16.[Medline] [Order article via Infotrieve]
10. Krahus JM. Structure of rat aortic baroreceptors and their relationship to connective tissue. J Neurocytol. 1979;8:401-414.[Medline] [Order article via Infotrieve]
11. Vargas da Silva S, Dias da Silva VJ, Ballejo G, Salgado MCO, Salgado HC. Blockers of the L-Arginine-nitric oxide-cyclic GMP pathway facilitate baroreceptor resetting. Hypertension. 1994;23(suppl I):I-60-I-63.
12. Dias da Silva VJ, Vargas da Silva S, Salgado MCO, Salgado HC. Chronic converting enzyme inhibition facilitates baroreceptor resetting to hypertensive levels. Hypertension. 1994;23(suppl I):I-68-I-72.
13. McDowell TS, Hajduczok G, Abboud FM, Chapleau MW. Baroreflex dysfunction in diabetes mellitus, II: site of baroreflex impairment in diabetic rabbits. Am J Physiol. 1994;266(Heart Circ Physiol. 35):H244-H249.
14. Rushton WAH. A theory of the effects of fiber
size in medullated nerve. J Physiol. 1951;115:101-122.
15. McDonald DM. Morphology of the rat carotid sinus nerve, II: number and size of axons. J Neurocytol. 1983;12:373-392.[Medline] [Order article via Infotrieve]
16. Sapru HN, Wang SC. Modification of aortic
baroreceptor resetting in the spontaneously hypertensive rat.
Am J Physiol. 1976;230:664-674.
17. Sapru HN, Krieger AJ. Role of receptor elements in baroreceptor resetting. Am J Physiol. 1979;236:H174-H182.[Medline] [Order article via Infotrieve]
18. Thomas PK. The connective tissue of peripheral nerve: an electron microscope study. J Anat Lond. 1963;97:35-44.
19. Gamble HJ. Comparative electron-microscopic observations on the connective tissues of a peripheral nerve and a spinal nerve root in the rat. J Anat [Lond]. 1964;98:17-25.
20. McDonald DM. Morphology of the rat carotid sinus nerve, I: course, connections, dimensions and ultrastructure. J Neurocytol. 1983;12:345-372.[Medline] [Order article via Infotrieve]
21. Schmidt EM, Stromberg MW. The myelinated fibers in the aortic nerve of the swine. Anat Rec. 1967;159:41-46.[Medline] [Order article via Infotrieve]
22. Friede RL, Beuche W. Combined scatter diagrams
of sheath thickness and fiber calibre in human sural nerves: changes
with age and neuropathy. J Neurol
Neurosurg Psychiatr. 1985;48:749-756.
23. Gasser HS. Properties of dorsal root
unmedullated fibers on the two sides of the ganglion.
J Gen Physiol. 1955;38:709-728.
24. Boyd IA, Kalu KU. Scaling factor relating
conduction velocity and diameter for myelinated afferent
nerve fibers in the cat hind limb. J Physiol. 1979;289:277-297.
25. Friede RL, Samorajski T. Relation between the number of myelin lamellae and axon circumference in fibers of vagus and sciatic nerves of mice. J Comp Neurol. 1967;130:223-232.[Medline] [Order article via Infotrieve]
26. Schoder JM. Altered ratio between axon diameter and myelin sheath thickness in regenerated nerve fibers. Brain Res. 1972;45:49-65.[Medline] [Order article via Infotrieve]
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