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Attenuation during paradoxical sleep of signals from tooth pulp to thalamus
Brain Research Bullerin,
Vol. 5, pp.
547-551.
Printed in the U.S.A.
Attenuation During Paradoxical Sleep of Signals from Tooth Pulp to Thalamus TOYOHIKO
SATOH, KUNIHIRO EGUCHI, KAZUSHIGE YOSHIO HARADA AND FUMIO HOTTA”
WATABE,
Department
of Physiology and 2nd Department of Oral Surgery*, School of Dental Medicine, Aichi-~akz~in University, Nagoya, 464, Japan Received
14 April 1980
SATOH, T., K. EGUCHI, K. WATABE, Y. HARADA AND F. HOTI’A. Atfenuation during pumdoxicai sleep ofsignals tooth puip to r~a~a~~~. BRAIN RES. BULL. 5(S) 547-551, 198O.~u~ti~tive evaluation of the response of thalamic neurons to tooth pulp st~ulation was made in chronically prepared cats. The latency, duration and intensity of the responses were measured from the post-stimulus time histograms to estimate, from various aspects, the alteration in the responsiveness during different phases of sleep and wakefulness. During slow wave sleep, tooth pulp-evoked impulses tended to be transmitted to the thalamus in a similar or slightly higher intensity compared to wakefulness. In contrast, during paradoxical sleep the signals were often attenuated in many aspects. The results seem to be in favor of the idea that the impairment of signal to noise ratio in a variety of neuronal networks is one of the characteristics of paradoxical sleep.
fLom
Tooth pulp
Pain
Thalamic neuron
Evoked response
THE sensation provoked by electrical stimulation of the human tooth pulp is predominantly, if not exclusively, pain 121. As the fiber composition of tooth pulp afferents in animals is comparable to that of man [3,5], electrical stimulation of the tooth pulp seems suitable for an experimental approach to the pain mechanism. Recently, different thalamic structures have been found to be involved in the transmission of tooth pulp-evoked impulses [6, 8, 9, 131. However, experiments conducted on behaving animals free from any drug and without serious surgical inte~ention are quite few f 1,4]. The present experiment was designed to quantitatively evaluate the responsiveness of thalamic neurons to tooth pulp stimulation in chronically prepared cats exhibiting a natural sleepwakefulness cycle. METHOD
Under pentobarbitone anesthesia (45 mglkg, IP) four adult cats were prepared for chronic experimentation. The unilateral maxillary canine tooth was drilled to implant bipolar stimulation electrodes. Spread of the stimulation current to the periodontal tissue was judged to be practically absent when no movement of the vibrissae or the facial musculature was visible upon the strong jaw opening reflex elicited by a high stimulation current. Leading wires were passed subcutaneously onto the skull and soldered to a socket to which the electrodes for recording the EEG, the nuchal muscle activity and the eye movements were also connected. A metal cylinder was fixed to the skull which was trepanned at the place dorsal to the thalamic region. The cylinder was used during recording to mount the stage for driving glassinsulated Pt-Ir microelectrode.
Copyright @ 1980 ANKHO
After a recovery period of 4 to 7 days, the head of the animal was restrained by clamping the acrylic mound on the skull. The tooth pulp was stimulated every 2 set by a train of 3 rectangular pulses of 0.01 msec duration and 1 msec interval at an intensity of 0.3-0.7 mA. These values were slightly above the threshold for jaw opening reflex occurring with a peak latency of 40-50 msec. At this intensity the animal never showed any sign of pain and exhibited normal sleep pattern. At an intensity several times higher, the stimulation seemed to be slightly unpleasant. This test was done only once because of ethical reasons. When a neuron apparently responding to tooth pulp stimulation was isolated, the movement of the jaw was restrained by applying a rod under it. The responses which were attentuated by this procedure were discarded as having been elicited by the activation of the receptors in the jaw closing muscles or the joint. At the end of the experiment, a stainless steel electrode was inserted stereotaxically under deep anesthesia into several recorded regions to make lesions electrolytically. The sites of recording were estimated in reference to those marks on serial sections stained with the Kllver-Barrera method. Data Analy~j~ The spike activity was, in parallel with sleep monitoring indices, recorded on magnetic tapes at a frequency response of 5 kHz, and analyzed with a data processor (Nihonkohden ATAC 2300). Post-stimulus time histograms (PSTHs) were constructed from 5&100 stimulation trials on each background; wakefulness (W), slow wave sleep (S) and paradoxical sleep (P). The mean latency, duration and intensity of the response were measured from the PSTH to calculate the
International Inc .-0361-9230/80/050547-05$01.00/O
SATOH 67 AL.
548
response magnitude (MAG), the response density (DENS), the information density (INF) and the modulation index (MOD): As illustrated in Fig. l-1. the MAG represents the number of evoked or suppressed spikes per single trial of stimulation. The DENS is the MAG per unit time of the response period (Fig. l-2). The INF is the product of the intensity of the response relative to the background discharge rate and the duration of the response relative to that during W. Therefore the INF would reflect the degree of contribution of the pulpal input to the output of the recorded neuron (Fig. l-3). The MOD represents the degree of deviation from W in terms of the latency, duration and MAG of the response during a given background:
MOD = / 1 -
latency relative1
duration + 11 -- relative1
to w
to w
1
.
response
magnitude
R-BG T
R@
BG@
2.
response
density
V.6 W
MAG + 11 -
relative1 to w -
In order to examine the correlative variation in the above-described parameters during different phases of sleep and wakefulness, various combinations of those parameters were displayed on the X-Y plotter.
3.
information R-
Ds -
density
TdFD: ._
RESULTS
Twenty-five neurons responded to tooth pulp stimulation with an increase and/or a decrease in the firing. Their location in the thalamus was, following the atlas of Jasper and Ajmone-Marsan 171, usually in the nucleus ventralis posterior medialis. Some neurons were in the nucleus centralis lateralis and in the posterior nucleus (Fig. 2). About two thirds of the neurons were contralateral to the stimulated tooth, and the rest ipsilateral. The response type was predominantly excitation-inhibition (n=12) or pure inhibition (n=7). In the remaining 6 neurons, there were 2 to 4 excitatory and/or inhibitory responses. A total of 29 excitatory and 20 inhibitory responses was obtained. The background discharge rate during S was lower than during W (S=O.573 W) in 14 out of 24 neurons. During P it was higher than W (P=2.385 W) in 9 out of 12 neurons. The latency during P was equal to or shorter than during W (P=O.568 W) in 14 out of 15 responses. The duration was, when compared with W, not shorter during S (S= 1.928 W) in 27 out of 42 responses and not longer during P (P=O.5’73 W) in 12 out of 15 responses. The MAG during S was almost comparable to W (Fig. 3A). During P the MAG was, in many cases, smaller than during W (Fig. 3B), and when compared ence was more conspicuous (Fig. 3C).
with S, the differ-
The DENS during W and S was similar in most responses (Fig. 4A). During P, the DENS tended to be smaller than during S (Fig. 4C), and this tendency was more obvious when compared with W (Fig. 4B). The INF during S tended to be greater than during W (Fig. SA). During P, the INF was definitely small in most cases as compared with both W and S (Fig. 5B and C). When the behavior during P or MAG, DENS and INF was examined with respect to the latency of the response, no systematic correlation was found. The MOD during S plotted against P indicated a trend that the response characteristics during P are more deviated from W than they are during S (Fig. 6).
output FIG. 1. 1: The formula and the scheme to calculate the MAG. R; number of spikes during excitatory (R,) or inhibitory (R,) response in the PSTH illustrated at the right. BG; number of background spikes (BG, or BG,) during corresponding responses. which was estimated from the mean backgrouid discharge-rate. T; number of stimulation trials utilized to make the PSTH. 2: The DENS. D; duration of the response in the PSTH during W, S or P. D,; duration during W. D,; duration during S. 3: The INF. tooth; the sector represents the intensity of tooth pulp-evoked impulses relative to the tota output of the recorded neuron during the response, and corresponds to the left half of the formula. The length of the cylinder as expressed by D/D, is the relative durability of this intensity during S or P.
DISCUSSION
The present results seem to indicate that during P the intensity of the thalamic response to signals from the tooth pulp is often reduced in many aspects, although the latency is sometimes shortened. During S, in contrast, the same signals tend to be transmitted in a similar or slightly higher intensity as compared with W. Although the stimulation apparently seemed not to be painful at the intensity employed in this experiment, it seems probable that the evoked impulses, at least those with a latency equal to or shorter than that for jaw opening reflex, are of pulpal origin and mediated through part of the channels used for encoding tooth pain, which could be provoked upon an intense stimulation. However, possible spread of stimulation currents to the periodontal tissue cannot be completely excluded, even at low stimulation intensity. Furthermore, it is possible that some of the evoked impulses are
THALAMIC
RESPONSE
549
TO TOOTH PULP IN SLEEP
FIG. 2. Localization of the recorded neurons of the frontal sections from A6.0 to AlO.0. Neurons driven by the contralateral tooth pulp are shown in the left of each figure with open circles. Solid circles in the right are ipsilaterally driven neurons.
related not to pain perception, but to activation of the efferent pathway of various reflex arcs. It has been suggested that at the moment of rapid eye movement burst during P the presynaptic inhibitory mechanism may be intensified at the terminals of the tooth pulp afferents in the spinal trigeminal nucleus [ 111. This inhibitory mechanism alone seems to be insufftcient in explaining the results during P obtained in the present experiment, because the mechanism was reported to be enhanced only sporadically. Signal transmission within the reticular structures of the lower brain stem has been shown to be often impaired during P fl0,12]. However, the depression of the thalamic
response during P does not seem to occur almost exclusively at the synapses in the reticular formation, but it may also occur to a considerable extent at the thalamic level, because the responses with short latency, which catmot be regarded as having been relayed through the reticular fo~ation, were depressed as often as those with long latency were. In conclusion, the present results on the thalamic neurons seem to be consistent with the observations in the lower afferent pathways, and to be in favor of the idea that the opulent of signal to noise ratio in a variety of neuronal networks is one of the characteristics of P.
550
SATOH
N /
B
2
z
4
0
/
o
3
1E
c/ 2
4
E,‘1 A I..
0
0
0
8
D
.
--/ ;
/
.!L:,:.,_,
MAGw
-o2
1
FIG. 3. MAC during W (MAG,), during S (MAG,) and during P (MAC,) were plotted reciprocally. Open circle; excitatoryresponse. Solid circle; inhibitory response. The oblique line with the sign of equality in A represents no difference in MAG between W and S, and the plots above this line have greater MAC during S than during W. All figures should be read in the same way.
/
. .
.
0
0
. / -*-.
.
. l
,
l
DENSw ,
t0
~
IO'
r-d-o$0
HENS H 00-m101
FIG. 4. DENS during W (DENS,.), during S (DENS.) and during P (DENS,,) plotted reciprocally.
0-.*-i lb
10'
FIG. 5. INF during W (INF,).
during S (INF,) and during P (INF,) plotted reciprocally.
DENS I
THALAMIC
RESPONSE
551
TO TOOTH PULP IN SLEEP
MODS
/,
I 1
0.1
10
FIG. 6. MOD during P (MOD,) plotted against MOD during S (MOD.). REFERENCES 1. Albe-Fessard, D., B. Nashold, B. Pollin and A. Woda. Thalamic and midbrain responses to dental pulp afferent messages in awake cats. .I. Physiol., Paris 73: 347-357, 1917. 2. Azerad, J. and A. Woda. Sensation evoked by bipolar _ intrapulpal stimulation in man. Pain 4: 145-152, 1977. 3. Beaslev, W. L. and G. R. Holland. A auantitative analvsis of the innervation of the pulp of the cat’s canine tooth. .I. camp. Neural. 178: 487-494, 1978. 4. Casey, K. L. Unit analysis of nociceptive mechanisms in the thalamus of the awake squirrel monkey. J. Neurophysiol. 29: 725-750, 1966. 5. Graf, W. and U. Hjelmquist. Caliber spectra of dental nerves in dogs and cattle. J. camp. Neurol. 103: 345-353. 1955. 6. Gmlbaud, G., D. Caillk, J. M. Besson and G.‘Benelli. Single units activities in ventral posterior and posterior group thalamic nuclei during nociceptive and non nociceptive stimulation in the cat. Archs ital. Biol. 115: 38-56, 1977. 7. Jasper, H. H. and C. Ajmone-Marsan. A Stereotaxic Atlas of the Diencephalon of the Cat. Ottawa: National Research Council of Canada, 1954.
8. Poggio, G. F. and V. B. Mountcastle. A study of the functional contributions of the ldmniscal and spinothalamic systems to somatic sensibility. Johns Hopkins Hosp. Bull. 106: 26316, 1960. 9. Ryu, H., W. K. Dong and I. H. Wagman. Cells in Pf, SPf and CL of thalamus respond only to noxious stimulation. Fedn Proc. 35: 561, 1976. 10. Satoh, T., K. Eguchi and K. Watabe. Functional relationship between cat brainstem neurons during sleep and wakefulness. Physiol. Behav. 22: 741-745,
1979.
11. Satoh, T., Y. Harada, K. Watabe, K. Eguchi and F. Hotta. Presynaptic inhibition of tooth pulp afferents in the trigeminal nucleushuring paradoxical sleep. sleep, in press, 1980.12. Satoh. T. and N. Kanamori. Reticula-reticular relationshin during sleep and waking. Physiol. Behav. 15: 333-337, 1975: 13. Woda, A., J. Azerad, G. Guilbaud et J. M. Besson. Etude microphysiologique des projections thahuniques de la pulpe dentaire chez le Chat. Brain Res. 89: 19>213, 1975.
Vol. 5, pp.
547-551.
Printed in the U.S.A.
Attenuation During Paradoxical Sleep of Signals from Tooth Pulp to Thalamus TOYOHIKO
SATOH, KUNIHIRO EGUCHI, KAZUSHIGE YOSHIO HARADA AND FUMIO HOTTA”
WATABE,
Department
of Physiology and 2nd Department of Oral Surgery*, School of Dental Medicine, Aichi-~akz~in University, Nagoya, 464, Japan Received
14 April 1980
SATOH, T., K. EGUCHI, K. WATABE, Y. HARADA AND F. HOTI’A. Atfenuation during pumdoxicai sleep ofsignals tooth puip to r~a~a~~~. BRAIN RES. BULL. 5(S) 547-551, 198O.~u~ti~tive evaluation of the response of thalamic neurons to tooth pulp st~ulation was made in chronically prepared cats. The latency, duration and intensity of the responses were measured from the post-stimulus time histograms to estimate, from various aspects, the alteration in the responsiveness during different phases of sleep and wakefulness. During slow wave sleep, tooth pulp-evoked impulses tended to be transmitted to the thalamus in a similar or slightly higher intensity compared to wakefulness. In contrast, during paradoxical sleep the signals were often attenuated in many aspects. The results seem to be in favor of the idea that the impairment of signal to noise ratio in a variety of neuronal networks is one of the characteristics of paradoxical sleep.
fLom
Tooth pulp
Pain
Thalamic neuron
Evoked response
THE sensation provoked by electrical stimulation of the human tooth pulp is predominantly, if not exclusively, pain 121. As the fiber composition of tooth pulp afferents in animals is comparable to that of man [3,5], electrical stimulation of the tooth pulp seems suitable for an experimental approach to the pain mechanism. Recently, different thalamic structures have been found to be involved in the transmission of tooth pulp-evoked impulses [6, 8, 9, 131. However, experiments conducted on behaving animals free from any drug and without serious surgical inte~ention are quite few f 1,4]. The present experiment was designed to quantitatively evaluate the responsiveness of thalamic neurons to tooth pulp stimulation in chronically prepared cats exhibiting a natural sleepwakefulness cycle. METHOD
Under pentobarbitone anesthesia (45 mglkg, IP) four adult cats were prepared for chronic experimentation. The unilateral maxillary canine tooth was drilled to implant bipolar stimulation electrodes. Spread of the stimulation current to the periodontal tissue was judged to be practically absent when no movement of the vibrissae or the facial musculature was visible upon the strong jaw opening reflex elicited by a high stimulation current. Leading wires were passed subcutaneously onto the skull and soldered to a socket to which the electrodes for recording the EEG, the nuchal muscle activity and the eye movements were also connected. A metal cylinder was fixed to the skull which was trepanned at the place dorsal to the thalamic region. The cylinder was used during recording to mount the stage for driving glassinsulated Pt-Ir microelectrode.
Copyright @ 1980 ANKHO
After a recovery period of 4 to 7 days, the head of the animal was restrained by clamping the acrylic mound on the skull. The tooth pulp was stimulated every 2 set by a train of 3 rectangular pulses of 0.01 msec duration and 1 msec interval at an intensity of 0.3-0.7 mA. These values were slightly above the threshold for jaw opening reflex occurring with a peak latency of 40-50 msec. At this intensity the animal never showed any sign of pain and exhibited normal sleep pattern. At an intensity several times higher, the stimulation seemed to be slightly unpleasant. This test was done only once because of ethical reasons. When a neuron apparently responding to tooth pulp stimulation was isolated, the movement of the jaw was restrained by applying a rod under it. The responses which were attentuated by this procedure were discarded as having been elicited by the activation of the receptors in the jaw closing muscles or the joint. At the end of the experiment, a stainless steel electrode was inserted stereotaxically under deep anesthesia into several recorded regions to make lesions electrolytically. The sites of recording were estimated in reference to those marks on serial sections stained with the Kllver-Barrera method. Data Analy~j~ The spike activity was, in parallel with sleep monitoring indices, recorded on magnetic tapes at a frequency response of 5 kHz, and analyzed with a data processor (Nihonkohden ATAC 2300). Post-stimulus time histograms (PSTHs) were constructed from 5&100 stimulation trials on each background; wakefulness (W), slow wave sleep (S) and paradoxical sleep (P). The mean latency, duration and intensity of the response were measured from the PSTH to calculate the
International Inc .-0361-9230/80/050547-05$01.00/O
SATOH 67 AL.
548
response magnitude (MAG), the response density (DENS), the information density (INF) and the modulation index (MOD): As illustrated in Fig. l-1. the MAG represents the number of evoked or suppressed spikes per single trial of stimulation. The DENS is the MAG per unit time of the response period (Fig. l-2). The INF is the product of the intensity of the response relative to the background discharge rate and the duration of the response relative to that during W. Therefore the INF would reflect the degree of contribution of the pulpal input to the output of the recorded neuron (Fig. l-3). The MOD represents the degree of deviation from W in terms of the latency, duration and MAG of the response during a given background:
MOD = / 1 -
latency relative1
duration + 11 -- relative1
to w
to w
1
.
response
magnitude
R-BG T
R@
BG@
2.
response
density
V.6 W
MAG + 11 -
relative1 to w -
In order to examine the correlative variation in the above-described parameters during different phases of sleep and wakefulness, various combinations of those parameters were displayed on the X-Y plotter.
3.
information R-
Ds -
density
TdFD: ._
RESULTS
Twenty-five neurons responded to tooth pulp stimulation with an increase and/or a decrease in the firing. Their location in the thalamus was, following the atlas of Jasper and Ajmone-Marsan 171, usually in the nucleus ventralis posterior medialis. Some neurons were in the nucleus centralis lateralis and in the posterior nucleus (Fig. 2). About two thirds of the neurons were contralateral to the stimulated tooth, and the rest ipsilateral. The response type was predominantly excitation-inhibition (n=12) or pure inhibition (n=7). In the remaining 6 neurons, there were 2 to 4 excitatory and/or inhibitory responses. A total of 29 excitatory and 20 inhibitory responses was obtained. The background discharge rate during S was lower than during W (S=O.573 W) in 14 out of 24 neurons. During P it was higher than W (P=2.385 W) in 9 out of 12 neurons. The latency during P was equal to or shorter than during W (P=O.568 W) in 14 out of 15 responses. The duration was, when compared with W, not shorter during S (S= 1.928 W) in 27 out of 42 responses and not longer during P (P=O.5’73 W) in 12 out of 15 responses. The MAG during S was almost comparable to W (Fig. 3A). During P the MAG was, in many cases, smaller than during W (Fig. 3B), and when compared ence was more conspicuous (Fig. 3C).
with S, the differ-
The DENS during W and S was similar in most responses (Fig. 4A). During P, the DENS tended to be smaller than during S (Fig. 4C), and this tendency was more obvious when compared with W (Fig. 4B). The INF during S tended to be greater than during W (Fig. SA). During P, the INF was definitely small in most cases as compared with both W and S (Fig. 5B and C). When the behavior during P or MAG, DENS and INF was examined with respect to the latency of the response, no systematic correlation was found. The MOD during S plotted against P indicated a trend that the response characteristics during P are more deviated from W than they are during S (Fig. 6).
output FIG. 1. 1: The formula and the scheme to calculate the MAG. R; number of spikes during excitatory (R,) or inhibitory (R,) response in the PSTH illustrated at the right. BG; number of background spikes (BG, or BG,) during corresponding responses. which was estimated from the mean backgrouid discharge-rate. T; number of stimulation trials utilized to make the PSTH. 2: The DENS. D; duration of the response in the PSTH during W, S or P. D,; duration during W. D,; duration during S. 3: The INF. tooth; the sector represents the intensity of tooth pulp-evoked impulses relative to the tota output of the recorded neuron during the response, and corresponds to the left half of the formula. The length of the cylinder as expressed by D/D, is the relative durability of this intensity during S or P.
DISCUSSION
The present results seem to indicate that during P the intensity of the thalamic response to signals from the tooth pulp is often reduced in many aspects, although the latency is sometimes shortened. During S, in contrast, the same signals tend to be transmitted in a similar or slightly higher intensity as compared with W. Although the stimulation apparently seemed not to be painful at the intensity employed in this experiment, it seems probable that the evoked impulses, at least those with a latency equal to or shorter than that for jaw opening reflex, are of pulpal origin and mediated through part of the channels used for encoding tooth pain, which could be provoked upon an intense stimulation. However, possible spread of stimulation currents to the periodontal tissue cannot be completely excluded, even at low stimulation intensity. Furthermore, it is possible that some of the evoked impulses are
THALAMIC
RESPONSE
549
TO TOOTH PULP IN SLEEP
FIG. 2. Localization of the recorded neurons of the frontal sections from A6.0 to AlO.0. Neurons driven by the contralateral tooth pulp are shown in the left of each figure with open circles. Solid circles in the right are ipsilaterally driven neurons.
related not to pain perception, but to activation of the efferent pathway of various reflex arcs. It has been suggested that at the moment of rapid eye movement burst during P the presynaptic inhibitory mechanism may be intensified at the terminals of the tooth pulp afferents in the spinal trigeminal nucleus [ 111. This inhibitory mechanism alone seems to be insufftcient in explaining the results during P obtained in the present experiment, because the mechanism was reported to be enhanced only sporadically. Signal transmission within the reticular structures of the lower brain stem has been shown to be often impaired during P fl0,12]. However, the depression of the thalamic
response during P does not seem to occur almost exclusively at the synapses in the reticular formation, but it may also occur to a considerable extent at the thalamic level, because the responses with short latency, which catmot be regarded as having been relayed through the reticular fo~ation, were depressed as often as those with long latency were. In conclusion, the present results on the thalamic neurons seem to be consistent with the observations in the lower afferent pathways, and to be in favor of the idea that the opulent of signal to noise ratio in a variety of neuronal networks is one of the characteristics of P.
550
SATOH
N /
B
2
z
4
0
/
o
3
1E
c/ 2
4
E,‘1 A I..
0
0
0
8
D
.
--/ ;
/
.!L:,:.,_,
MAGw
-o2
1
FIG. 3. MAC during W (MAG,), during S (MAG,) and during P (MAC,) were plotted reciprocally. Open circle; excitatoryresponse. Solid circle; inhibitory response. The oblique line with the sign of equality in A represents no difference in MAG between W and S, and the plots above this line have greater MAC during S than during W. All figures should be read in the same way.
/
. .
.
0
0
. / -*-.
.
. l
,
l
DENSw ,
t0
~
IO'
r-d-o$0
HENS H 00-m101
FIG. 4. DENS during W (DENS,.), during S (DENS.) and during P (DENS,,) plotted reciprocally.
0-.*-i lb
10'
FIG. 5. INF during W (INF,).
during S (INF,) and during P (INF,) plotted reciprocally.
DENS I
THALAMIC
RESPONSE
551
TO TOOTH PULP IN SLEEP
MODS
/,
I 1
0.1
10
FIG. 6. MOD during P (MOD,) plotted against MOD during S (MOD.). REFERENCES 1. Albe-Fessard, D., B. Nashold, B. Pollin and A. Woda. Thalamic and midbrain responses to dental pulp afferent messages in awake cats. .I. Physiol., Paris 73: 347-357, 1917. 2. Azerad, J. and A. Woda. Sensation evoked by bipolar _ intrapulpal stimulation in man. Pain 4: 145-152, 1977. 3. Beaslev, W. L. and G. R. Holland. A auantitative analvsis of the innervation of the pulp of the cat’s canine tooth. .I. camp. Neural. 178: 487-494, 1978. 4. Casey, K. L. Unit analysis of nociceptive mechanisms in the thalamus of the awake squirrel monkey. J. Neurophysiol. 29: 725-750, 1966. 5. Graf, W. and U. Hjelmquist. Caliber spectra of dental nerves in dogs and cattle. J. camp. Neurol. 103: 345-353. 1955. 6. Gmlbaud, G., D. Caillk, J. M. Besson and G.‘Benelli. Single units activities in ventral posterior and posterior group thalamic nuclei during nociceptive and non nociceptive stimulation in the cat. Archs ital. Biol. 115: 38-56, 1977. 7. Jasper, H. H. and C. Ajmone-Marsan. A Stereotaxic Atlas of the Diencephalon of the Cat. Ottawa: National Research Council of Canada, 1954.
8. Poggio, G. F. and V. B. Mountcastle. A study of the functional contributions of the ldmniscal and spinothalamic systems to somatic sensibility. Johns Hopkins Hosp. Bull. 106: 26316, 1960. 9. Ryu, H., W. K. Dong and I. H. Wagman. Cells in Pf, SPf and CL of thalamus respond only to noxious stimulation. Fedn Proc. 35: 561, 1976. 10. Satoh, T., K. Eguchi and K. Watabe. Functional relationship between cat brainstem neurons during sleep and wakefulness. Physiol. Behav. 22: 741-745,
1979.
11. Satoh, T., Y. Harada, K. Watabe, K. Eguchi and F. Hotta. Presynaptic inhibition of tooth pulp afferents in the trigeminal nucleushuring paradoxical sleep. sleep, in press, 1980.12. Satoh. T. and N. Kanamori. Reticula-reticular relationshin during sleep and waking. Physiol. Behav. 15: 333-337, 1975: 13. Woda, A., J. Azerad, G. Guilbaud et J. M. Besson. Etude microphysiologique des projections thahuniques de la pulpe dentaire chez le Chat. Brain Res. 89: 19>213, 1975.