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Ascending sensory pathways from the genitalia of the cat
EXPERIMENTAL
NEUROLOGY
Ascending
2, 186-190
Sensory
MAURICE
MEYER,
Departments Minnesota,
of Physiology and Laboratory Los Angeles
EUGENE
(1960)
Pathways from of the Cat SCHRAE LAPLANTE,
the Genitalia AND BERRY CAMPBELL~
and Anatomy, University of Minnesota, of Neurological Research, College of Medical County Hospital, Los Angeles, Cakfornia Received
December
Minneapolis, Evangelists,
28, 1959
Ascending sensory pathways from the genitalia in the spinal cord and brain stem were followed in cats, using single shock stimuli. Animals were anesthetized with Dial or Nembutal. Tract and nuclear potentials were studied with cathoderay oscillography. Compared with ascending pathways from the tibia1 nerve, the spinal tracts, including dorsal column, ipsilateral column (presumably Flechsig’s tract), and the contralateral column (spinothalamic tract) from the pudendal nerve field showed conduction patterns which were slower, less in amplitude, and of less abrupt rising phase. A correlation of the speed of conduction of the secondary fibers in the spinal cord with that of the corresponding primary peripheral nerves is detected. Signal from the rapidly conducting fibers of the tibia1 nerve is transferred to spinal ascending fibers of rapid conduction velocity, while signal from the more slowly conducting pudendal nerve fibers ascends the spinal cord more slowly. Introduction
In two previous communications (1, 2) pathways of sexual stimuli from the genitalia were discussedwith regard to anatomy of the end organs, fiber-size spectra of peripheral nerves, patterns of primary sensory stimuli, and reactions in the third and fourth sacral segments. In the present report, the conduction within the spinal cord of signals delivered to the genitalia or to the pudendal nerve was examined. As in the former studies, specifically L‘sexuaI” stimuli were not used except inasmuch as the nerves to the genitalia were stimulated. The pathways activated were thus not necessarily the ones which transmit stimuli of sexual sign per se, but we may expect that they were the ones which formed the most direct and 1 Aided by a grant from The Committee for Research in the Problems of Sex, National Academy of Sciences. The senior author holds a postdoctoral Public Health Service Research Fellowship of the National Institute of Dental Research. 186
SENSORY
PATHS
FROM
GENITALIA
187
rapid pathways for sensation from the genitalia. In the data presented we have attempted to delineate routes, conduction speeds, and patterns of the ascending signal. In a previous paper (2)) the nature of the compound action potential in genital nerves was examined and analyzed with reference to fiber size spectra. Materials
and
Methods
In this study, 36 cats (22 males, 14 females) were used. They were anesthetized with Dial or Nembutal (about 0.7 mg/kg) Biopotentials were studied with a cathode-ray oscillograph after surgical exposure of the spinal cord and the lower part of the brain stem. Recording electrodes were made by drawing glass capillaries filled with silver solder. These varied in diameter from 25 to 75 p. They were mounted on a three-way vernier electrode holder. Oscillographic tracings were made of potential differences between the microelectrode and a large “indifferent” electrode on nearby inactive tissue. Stimuli were delivered to two sites for the genital stimulation. Silver wire bipolar electrodes were placed across the glans penis or on the vulva in the region of the glans clitoridis. In other experiments, the tibia1 nerve at the popliteal space was sectioned and similarly stimulated for comparison. Observations
Effectiveness of the direct stimulation of genitalia by single shocks was determined by examining activity in the corresponding S3 dorsal rootlets. Deflection evoked by stimulation of the penis is illustrated in Fig. 1A. There were constant differences between potentials evoked by stimulation of the genitalia directly or by stimulation of the central cut end of the pudendal nerve, on one hand, and potentials evoked by tibia1 nerve stimulation on the other. The pudendal nerve field was apparently deficient in fast conducting receptor fibers, and resulting potentials at the dorsal rootlets were delayed and showed a less abrupt commencement. Amplitude was low compared with the corresponding tibia1 nerve potentials. Thus the signal as delivered by compound action potential to the spinal cord differed in the case of the pudendal nerve pathway from that of the tibia1 nerve. A lower amplitude and less abrupt onset was seen in activity within the spinal cord not only in the dorsal column of the local segments (contrast Figs. 1C and lD), but also in the dorsal column records at Cl (contrast Figs. 2A and 2C with 2B). Average conduction
188
MEYER,
LA PLANTE,
AND
CAMPBELL
velocity in the pudendal nerve was 39 m per second; in the tibia1 nerve, 68 m per second. Direct conduction in the dorsal column at Cl was obtained a number of times in these experiments. Representative traces of activity are shown in Fig. 2. Average conduction velocity from the pudendal nerve field was 41 m per second, from tibia1 field, 53 m per second. Indirect or relayed activity from genitalia and tibia1 field was recorded and measured in the lateral columns. Ipsilateral activity of the dorsal spinocerebellar pathway
FIG. 1. Recordings from: (A) dorsal rootlets, S3; stimulation, penis. (B) rootlets, S3 ; stimulation, tibia1 nerve. (C) dorsum of cord, Sl ; stimulation, (D) dorsum of cord, Sl; stimulation, tibia1 nerve. Time in milliseconds.
2. Recordings from dorsal stimulation, tibia1 nerve. (C)
FIG.
(B)
column at Cl: (A) stimulation, pudendal stimulation, penis. Time in milliseconds.
dorsal penis.
nerve.
SENSORY
PATHS
FROM
GENITALIA
189
was clocked at high conduction velocities characteristic of this pathway. From the data of these experiments, actual velocities within the spinal cord can be calculated only in the instance of one animal, in which the activity in response to stimulation of the vulva and tibia1 nerve was recorded in the ipsilateral column at Cl (one pudendal nerve had been sectioned previously). Correcting for peripheral conduction latencies and distances given for this animal, and allowing 0.9 msec for synaptic delay, the velocities within the contralateral column for pudendal and tibia1 activity were calculated to be 70 m per second and 130 m per second respectively, compared with dorsal column conduction velocities of 41 m per second and 55 m per second, obtained in a like manner. These values for the tibia1 nerve lie within the range of velocities reported by Grundfest and Campbell (3). The slower velocity of the dorsal column fibers serving the pudendal nerve has been mentioned above. It is remarkable that the calculated velocity of the conducted activity within the secondary tract, presumably the dorsal spinocerebellar fasciculus was so much slower from the genital nerve field than the tibia1 nerve field. Our records for pudendal nerve activity in the contralateral column showed an average conduction velocity of 34 m per second (variation, 3&35), for tibia1 nerve records, 48 m per second (variation, 43-61). This is significantly faster than conduction velocities reported by Collins and Randt (4) in the cat, but slower than figures presented by Correa and Grundfest (5) for tract conduction in this region of the monkey. The reason for this discrepancy is not apparent, but our experiments were not exactly comparable to those of the previous authors. The rather wide difference between the conduction velocity which we measured for activity evoked in this column by pudendal nerve (or genitalia) stimulation and that following stimuli to the tibia1 nerve agreed with the observations presented above concerning the difference in velocity of these two systems in the dorsal and ipsilateral columns. Discussion
These experiments demonstrate that activity evoked by stimulation of the pudendal nerve field in ascending sensory tracts and related nuclei are distinguished by their increased latencies, lower amplitudes, slower rising time, and more restricted distribution than their “tibia1 controls.” There is little doubt that these properties are, for the most part, correlated with the special sensory mode of the genital field, and lo- to 14-p nerve fibers which characterize these afferents. Both the pudendal and
190
MEYER,
LA PLANTE,
AND
CAMPBELL
tibia1 nerve contain general sensory componentswith the peak of fibers in the 4- to 6-p diameter range. It is the nature of these experiments, however, that they reveal most clearly activities related to the faster fibers present in the nerves. In the case of the pudendal nerve, these are the lo- to 14-p group related to encapsulatedend organs in the phallus. The tibia1 nerve, on the other hand, contains a more rapidly conducting component of afferent fibers in the 14- to 18-p range, presumably muscle afferents (6). There is a difference in conduction velocities in afferents of the glans clitoridis and striated muscleof the vulva, the latter being much faster (2). Perhaps the most unexpected finding in these studies is that conduction velocities in the spinal cord, dorsal, ipsilateral, and contralateral lateral columns, are very much slower for pudendal nerve or genital activity than for tibia1 nerve activity. Fibers of the dorsal columns are, of course, central fibers of primary sensory neurons and it is not so surprising to find that their conduction velocity is matched to that of their peripheral fibers. These findings imply that signal in the secondary ascending tracts is carried on fibers somewhat matched in diameter to those of the peripheral conductors. References 1.
2.
3.
4. 5.
6.
CAMPBELL, B., C. A. GOOD, and R. L. KUCHELL, Neural mechanisms in sexual behavior. I. Reflexology of sacral segment of cat. Proc. Sot. Exp. Biol., N. Y. 86: 423-426, 1954. KITCHELL, R. L., B. CAMPBELL, T. A. QVILLIAM, and L. L. LARSON, Neurological factors in the sexual behavior of domestic animals. “Proceedings Book,” Am. Vet. M. Ass., 92nd Ann. Meeting, pp. 177-189, 1955. GRUNDFEST, H., and B. CAMPBELL, Origin, conduction and termination of impulses in dorsal spinocerebellar tracts of cats. J. NeurophysioL 5: 275-294, 1942. COLLINS, W. F., and C. T. RANDT, An electrophysiological study of small myelinated axons in anterolateral column in cat. J. Neurophysiol. 19: 438445, 1956. CORREA, R. M. E., and H. GRUNDFEST, Electrophysiological studies of cerebellar inflow. I. Origin, conduction and termination of ventral spino-cerebellar tract in monkey and cat. J. Neurophysiol. 17: 208-238, 1954. QVILLIAM, T. A., Some characteristics of myelinated fibre populations. J. Anat., Lond. 90: 172-187, 1956.
NEUROLOGY
Ascending
2, 186-190
Sensory
MAURICE
MEYER,
Departments Minnesota,
of Physiology and Laboratory Los Angeles
EUGENE
(1960)
Pathways from of the Cat SCHRAE LAPLANTE,
the Genitalia AND BERRY CAMPBELL~
and Anatomy, University of Minnesota, of Neurological Research, College of Medical County Hospital, Los Angeles, Cakfornia Received
December
Minneapolis, Evangelists,
28, 1959
Ascending sensory pathways from the genitalia in the spinal cord and brain stem were followed in cats, using single shock stimuli. Animals were anesthetized with Dial or Nembutal. Tract and nuclear potentials were studied with cathoderay oscillography. Compared with ascending pathways from the tibia1 nerve, the spinal tracts, including dorsal column, ipsilateral column (presumably Flechsig’s tract), and the contralateral column (spinothalamic tract) from the pudendal nerve field showed conduction patterns which were slower, less in amplitude, and of less abrupt rising phase. A correlation of the speed of conduction of the secondary fibers in the spinal cord with that of the corresponding primary peripheral nerves is detected. Signal from the rapidly conducting fibers of the tibia1 nerve is transferred to spinal ascending fibers of rapid conduction velocity, while signal from the more slowly conducting pudendal nerve fibers ascends the spinal cord more slowly. Introduction
In two previous communications (1, 2) pathways of sexual stimuli from the genitalia were discussedwith regard to anatomy of the end organs, fiber-size spectra of peripheral nerves, patterns of primary sensory stimuli, and reactions in the third and fourth sacral segments. In the present report, the conduction within the spinal cord of signals delivered to the genitalia or to the pudendal nerve was examined. As in the former studies, specifically L‘sexuaI” stimuli were not used except inasmuch as the nerves to the genitalia were stimulated. The pathways activated were thus not necessarily the ones which transmit stimuli of sexual sign per se, but we may expect that they were the ones which formed the most direct and 1 Aided by a grant from The Committee for Research in the Problems of Sex, National Academy of Sciences. The senior author holds a postdoctoral Public Health Service Research Fellowship of the National Institute of Dental Research. 186
SENSORY
PATHS
FROM
GENITALIA
187
rapid pathways for sensation from the genitalia. In the data presented we have attempted to delineate routes, conduction speeds, and patterns of the ascending signal. In a previous paper (2)) the nature of the compound action potential in genital nerves was examined and analyzed with reference to fiber size spectra. Materials
and
Methods
In this study, 36 cats (22 males, 14 females) were used. They were anesthetized with Dial or Nembutal (about 0.7 mg/kg) Biopotentials were studied with a cathode-ray oscillograph after surgical exposure of the spinal cord and the lower part of the brain stem. Recording electrodes were made by drawing glass capillaries filled with silver solder. These varied in diameter from 25 to 75 p. They were mounted on a three-way vernier electrode holder. Oscillographic tracings were made of potential differences between the microelectrode and a large “indifferent” electrode on nearby inactive tissue. Stimuli were delivered to two sites for the genital stimulation. Silver wire bipolar electrodes were placed across the glans penis or on the vulva in the region of the glans clitoridis. In other experiments, the tibia1 nerve at the popliteal space was sectioned and similarly stimulated for comparison. Observations
Effectiveness of the direct stimulation of genitalia by single shocks was determined by examining activity in the corresponding S3 dorsal rootlets. Deflection evoked by stimulation of the penis is illustrated in Fig. 1A. There were constant differences between potentials evoked by stimulation of the genitalia directly or by stimulation of the central cut end of the pudendal nerve, on one hand, and potentials evoked by tibia1 nerve stimulation on the other. The pudendal nerve field was apparently deficient in fast conducting receptor fibers, and resulting potentials at the dorsal rootlets were delayed and showed a less abrupt commencement. Amplitude was low compared with the corresponding tibia1 nerve potentials. Thus the signal as delivered by compound action potential to the spinal cord differed in the case of the pudendal nerve pathway from that of the tibia1 nerve. A lower amplitude and less abrupt onset was seen in activity within the spinal cord not only in the dorsal column of the local segments (contrast Figs. 1C and lD), but also in the dorsal column records at Cl (contrast Figs. 2A and 2C with 2B). Average conduction
188
MEYER,
LA PLANTE,
AND
CAMPBELL
velocity in the pudendal nerve was 39 m per second; in the tibia1 nerve, 68 m per second. Direct conduction in the dorsal column at Cl was obtained a number of times in these experiments. Representative traces of activity are shown in Fig. 2. Average conduction velocity from the pudendal nerve field was 41 m per second, from tibia1 field, 53 m per second. Indirect or relayed activity from genitalia and tibia1 field was recorded and measured in the lateral columns. Ipsilateral activity of the dorsal spinocerebellar pathway
FIG. 1. Recordings from: (A) dorsal rootlets, S3; stimulation, penis. (B) rootlets, S3 ; stimulation, tibia1 nerve. (C) dorsum of cord, Sl ; stimulation, (D) dorsum of cord, Sl; stimulation, tibia1 nerve. Time in milliseconds.
2. Recordings from dorsal stimulation, tibia1 nerve. (C)
FIG.
(B)
column at Cl: (A) stimulation, pudendal stimulation, penis. Time in milliseconds.
dorsal penis.
nerve.
SENSORY
PATHS
FROM
GENITALIA
189
was clocked at high conduction velocities characteristic of this pathway. From the data of these experiments, actual velocities within the spinal cord can be calculated only in the instance of one animal, in which the activity in response to stimulation of the vulva and tibia1 nerve was recorded in the ipsilateral column at Cl (one pudendal nerve had been sectioned previously). Correcting for peripheral conduction latencies and distances given for this animal, and allowing 0.9 msec for synaptic delay, the velocities within the contralateral column for pudendal and tibia1 activity were calculated to be 70 m per second and 130 m per second respectively, compared with dorsal column conduction velocities of 41 m per second and 55 m per second, obtained in a like manner. These values for the tibia1 nerve lie within the range of velocities reported by Grundfest and Campbell (3). The slower velocity of the dorsal column fibers serving the pudendal nerve has been mentioned above. It is remarkable that the calculated velocity of the conducted activity within the secondary tract, presumably the dorsal spinocerebellar fasciculus was so much slower from the genital nerve field than the tibia1 nerve field. Our records for pudendal nerve activity in the contralateral column showed an average conduction velocity of 34 m per second (variation, 3&35), for tibia1 nerve records, 48 m per second (variation, 43-61). This is significantly faster than conduction velocities reported by Collins and Randt (4) in the cat, but slower than figures presented by Correa and Grundfest (5) for tract conduction in this region of the monkey. The reason for this discrepancy is not apparent, but our experiments were not exactly comparable to those of the previous authors. The rather wide difference between the conduction velocity which we measured for activity evoked in this column by pudendal nerve (or genitalia) stimulation and that following stimuli to the tibia1 nerve agreed with the observations presented above concerning the difference in velocity of these two systems in the dorsal and ipsilateral columns. Discussion
These experiments demonstrate that activity evoked by stimulation of the pudendal nerve field in ascending sensory tracts and related nuclei are distinguished by their increased latencies, lower amplitudes, slower rising time, and more restricted distribution than their “tibia1 controls.” There is little doubt that these properties are, for the most part, correlated with the special sensory mode of the genital field, and lo- to 14-p nerve fibers which characterize these afferents. Both the pudendal and
190
MEYER,
LA PLANTE,
AND
CAMPBELL
tibia1 nerve contain general sensory componentswith the peak of fibers in the 4- to 6-p diameter range. It is the nature of these experiments, however, that they reveal most clearly activities related to the faster fibers present in the nerves. In the case of the pudendal nerve, these are the lo- to 14-p group related to encapsulatedend organs in the phallus. The tibia1 nerve, on the other hand, contains a more rapidly conducting component of afferent fibers in the 14- to 18-p range, presumably muscle afferents (6). There is a difference in conduction velocities in afferents of the glans clitoridis and striated muscleof the vulva, the latter being much faster (2). Perhaps the most unexpected finding in these studies is that conduction velocities in the spinal cord, dorsal, ipsilateral, and contralateral lateral columns, are very much slower for pudendal nerve or genital activity than for tibia1 nerve activity. Fibers of the dorsal columns are, of course, central fibers of primary sensory neurons and it is not so surprising to find that their conduction velocity is matched to that of their peripheral fibers. These findings imply that signal in the secondary ascending tracts is carried on fibers somewhat matched in diameter to those of the peripheral conductors. References 1.
2.
3.
4. 5.
6.
CAMPBELL, B., C. A. GOOD, and R. L. KUCHELL, Neural mechanisms in sexual behavior. I. Reflexology of sacral segment of cat. Proc. Sot. Exp. Biol., N. Y. 86: 423-426, 1954. KITCHELL, R. L., B. CAMPBELL, T. A. QVILLIAM, and L. L. LARSON, Neurological factors in the sexual behavior of domestic animals. “Proceedings Book,” Am. Vet. M. Ass., 92nd Ann. Meeting, pp. 177-189, 1955. GRUNDFEST, H., and B. CAMPBELL, Origin, conduction and termination of impulses in dorsal spinocerebellar tracts of cats. J. NeurophysioL 5: 275-294, 1942. COLLINS, W. F., and C. T. RANDT, An electrophysiological study of small myelinated axons in anterolateral column in cat. J. Neurophysiol. 19: 438445, 1956. CORREA, R. M. E., and H. GRUNDFEST, Electrophysiological studies of cerebellar inflow. I. Origin, conduction and termination of ventral spino-cerebellar tract in monkey and cat. J. Neurophysiol. 17: 208-238, 1954. QVILLIAM, T. A., Some characteristics of myelinated fibre populations. J. Anat., Lond. 90: 172-187, 1956.