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Observations on facial nociception in a monkey after destruction of the rostral part of the trigeminal sensory nuclear complex
129
Pain, 21 (1985) 129-135 Elsevier
PA1 00712
Observations on Facial Nociception in a Monkey after Destruction of the Rostra1 Part of the Trigeminal Sensory Nuclear Complex S.J.W. Lisney Department of Physiology (Oral Biology), The Medico1 School, University Walk, Bristol BS8 I TD (U.K.) (Received
15 March 1984, accepted
26 September
1984)
Summary Facial sensibility was assessed in a cynomolgus monkey in whom the trigeminal main sensory nucleus and the rostral part of the trigeminal nucleus oralis on one side had been destroyed. The animal responded equally to noxious mechanical stimuli applied to the two sides of the face; no deficiency in nociception could be detected. This finding suggests that the synaptic connections made by nociceptor afferents from the face in rostra1 parts of the trigeminal sensory nuclear complex are not essential for facial nociception. These observations are also consistent with the opinion that, from a functional point of view, facial nociceptor afferents have their principal synaptic connections in the nucleus caudalis of the trigeminal spinal complex.
Introduction In both man and animals, destruction of the caudal part of the trigeminal spinal complex results in a complete or partial loss of pain and temperature sensation on the side of the face ipsilateral to the lesion, with little or no loss of tactile sensibility (for information on man, see refs. 4, 5; on animals, see refs. 2, 3, 6, 11, 13). Those who made the first observations of this sort suggested that the nucleus caudalis was the synaptic station for sensory nerve fibres involved in facial nociception and, since touch and pressure sensibility were preserved, that sensory fibres signalling information about tactile stimulation of the face synapsed with higher order neurones in rostral parts of the trigeminal sensory nuclear complex, particularly the trigeminal 0304-3959/85/%03.30
0 1985 Elsevier Science Publishers
B.V. (Biomedical
Division)
130
main sensory nucleus. This proposal that there were functional subdivisions within the trigeminal sensory nuclear complex became widely accepted and it formed the basis of the rationale behind Sjoquist’s trigeminal tractotomy operation for the relief of persistent trigeminal pain [9]. The clinical results that he and others achieved supported the concept of functional subdivisions within the nuclear complex, and many still hold this view. An alternative view of how the trigeminal sensory nuclear complex may be organized was put forward by Wall and Taub [12], and more recently Denny-Brown and Yanagisawa [2] have taken up this idea and expressed it in more detail. The proposal is that there are no strict functional subdivisions within the complex, but instead the important feature is the neural output of the complex as a whole. For sensations to be perceived. the neural output from the complex to some higher part of the central nervous system has to reach particular critical levels; the critical level of nervous activity needed for pain is higher than that for temperature sensation and this in turn is higher than the level of activity necessary for touch. With this theory the deficiencies in facial sensibility experienced after destruction of the caudal part of the nuclear complex are accounted for in terms of loss of output from the complex as a whole following damage to part of it rather than in terms of destruction of a specific set of synaptic connections. If this view is correct, one would expect localized destruction of some other part of the nuclear complex to result in an ipsilateral loss of pain sensibility but if the more established view is correct, such a lesion should leave facial pain sensibility unaltered. The experiments described here were carried out to see which of these two possibilities occurred following localized lesions in rostra1 parts of the trigeminal sensory nuclear complex.
Methods
Six feral, male cynomolgus monkeys (Mucaca f~cjcu~arj~} weighing between 3.5 and 5.5 kg were used in the experiments. Over a period of several months they were trained to leave their cages and sit in a restraint chair where they were introduced to the procedures that later would be used to test facial sensibility. The method used was based on that described by Denny-Brown and Yanagisawa [2] in their study of facial nociception in monkeys; additional practical advice was obtained from correspondence with Dr. Denny-Brown. It involved stimulating the face and head by stroking and pressing the skin with a blunt ended plastic rod, displacing a few hairs with the rod, and pricking and scratching with a pin fixed into the end of a second, similar rod. A movement of the animal, whether the movement was of the whole head away from the source of the stimulus or just a slight movement of the facial musculature, was taken as an indication that the animal had perceived the stimulus. Occasionally the animals would make threatening gestures, baring their teeth, for example, in response to noxious stimuli. Both sides of the head and face were tested so that responses following stim~ation on the experimental side could be compared with those to the same stimulus on the normal side. None of the animals would allow testing in or around the mouth and the design of the restraint chair was such
131
that skin under the chin and lower jaw could not be tested satisfactorily. Each testing session lasted 25-35 min, during which rewards of fruit were given periodically. One animal did not tolerate these procedures and it had to be eliminated from the project. Once the monkeys were accustomed to facial sensibility testing, a brief operation was carried out in which stereotaxic, electrolytic lesions were made in rostra1 parts of the left t~ge~nal sensory nuclear complex. The animals were anaesthetized with ketamine hydrochloride (20 mg/kg i.m.) followed by sodium pentobarbitone (24 mg/kg i.p.) and then placed in a Kopf stereotaxic frame. The scalp and temporalis muscle on the left side were reflected, a small hole made in the cranium at the appropriate place, and the lesioning electrode positioned in the trigeminal main sensory nucleus and/or the nucleus oralis of the spinal trigeminal complex (Olszewski’s terminology [7]), using stereotaxic coordinates from the atlas of Shantha et al. (81. Lesions were made by passing DC current (5 mA, 30 set) between the tip of the electrode (anode) and an indifferent electrode attached to a saline soaked pad on the exposed temporalis muscle. Lesions were made at several adjacent sites in each animal. The muscle and skin wounds were sutured separately, an intramuscular injection of penicillin given and then the animals were allowed to recover. Testing of facial sensation began again 4-7 days after the operation and continued several times a week for 4-6 weeks. At the end of this period the animals were re-anaesthetized and perfused via both carotid arteries with 1 litre of Ringer’s solution with 1% procaine as a pre-wash followed by 3 litres of phosphate-buffered formaldehyde fixative. Each brain was left in fixative for a further 1 or 2 weeks and then 80 pm serial, frozen sections were cut from the brain-stem for histological identification of the lesion sites.
Because of variation in brain size from animal to animal, it is difficult to make stereotaxic lesions with pin-point accuracy [lo]. In 2 of the 5 animals the lesions produced were misplaced, in 2 animals the lesions destroyed only parts of the trigeminal main sensory nucleus or the nucleus orahs, and in 1 animal the main sensory nucleus and the rostra1 part of nucleus oralis appeared to be completely destroyed. The positions of the lesions in these last 3 monkeys are shown in Fig. 1. Animal D was the one in which all the main sensory nucleus and some of the rostral part of nucleus oralis were destroyed; most of the trigeminal descending spinal tract was spared, being just lateral to the lesion, but some of the medial part was damaged. Parts of the trigeminal motor nucleus and the nucleus of the facial nerve were also involved in the lesion; this was anticipated as there was wasting of the temporalis and masseter muscles and paralysis of some of the facial muscles on the lesioned side. The lesion extended more dorsally than planned, involving cerebellar pathways, and the animal showed some locomotor disability as a consequence. Despite these complications, the animal ate normally, it learned to cope with its lack of motor coordination and it continued to cooperate in the experiment.
132 ANIMAL
8
._ _j L ,‘OI. (’
ANIMAL
C
ANIMAL
0
2’
PY ; ’
-10 8
6
4
2
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8
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-10
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133
Testing of facial sensibility in monkey D failed to reveal any difference in the response to noxious mechanical stimulation (pin-prick, pin-scratch) between the normal and operated sides of the face. The usual response to a noxious stimulus was a brisk turning of the head away from the direction of stimulation; occasionally the animal would frown, as if in disapproval, or make a threatening gesture. Alarm calls were not made. These responses were not observed when the blunt plastic rod was used to apply non-noxious mechanical stimuli to the same areas of the face and so it seems unlikely that visual clues were important in eliciting these responses. The same results were obtained with the 2 animals, monkeys B and C, in which there was only partial destruction of the rostra1 part of the trigeminal sensory nuclear complex. It was more difficult to make decisions about responses to non-noxious stimulation of the face. Before their operation all the animals had become accustomed to having their faces and heads stroked, touched and pressed by a blunt plastic rod and they seemed to be indifferent to this type of stimulation. If, however, just a few of the longer guard hairs were displaced, the animals would occasionally respond with a slight jerk of the head or a twitch of an adjacent facial muscle. The impression gained was that this type of light, tactile stimulation was irritating, like a fly walking across the skin. After the lesion operations the animals showed the same indifference to touch and light pressure but in animals B and D, where there was some paralysis of the facial musculature, it was more difficult to detect responses to movements of guard hairs.
Discussion
From the outset it must be said that although the methods used to test facial sensation were essentially those used in clinical neurological examinations, they are relatively crude and can only give an impression of facial sensibility. This is particularly so when used with animals, where the investigator has to make an assessment on the evidence of outward signs alone and the subject cannot give additional verbal information. It may well be that there were subtle changes in facial
-~
--.
Fig. 1. Diagrams showing the positions of the lesions in monkeys B, C and D. On the right are dorsal views of the brain-stem showing the antero-posterior position of each lesion in relation to the Horsley-Clark stereotaxic coordinates; the diagrams were drawn using information from the atlases of Shantha et al. [8] and Szabo and Cowan [lo]. The stippling shows the positions of the trigeminal main sensory nucleus and the trigeminal spinal complex. Olszewski [7] states that in the trigeminal spinal complex, the transition from the nucleus interpolar6 to the nucleus oralis takes place at the level of the oral third of the inferior olive; in this diagram this would be between AP -0.5 and iO.5. In each diagram the cross-hatching indicates the extent of the lesion. On the left are drawings made from coronal sections of the brain-stem showing the individual lesion sites at the AP levels indicated by the arrows. Abbreviations (using the nomenclature of Shantha et al. [8]): BC, bra&urn conjunctivum; DR, nucleus dorsalis raphe; NF, nucleus n. facialis; NMA, nucleus medialis anuli aquaeducti; NMV, nucleus motorius n. trigemini; NW, nucleus tractus spinalis n. trigemini; 01, nucleus olivaris inferior; PVA, nucleus principalis n. trigeminalis; PY, tractus pyrimidalis; TSV, tractus spinalis n. trigemini.
134
sensation in these lesioned animals that went undetected. Although it would have been possible to devise more sophisticated methods of testing facial sensibility, it was decided to use these more simple procedures so that the results obtained would be directly comparable with those obtained by Denny-Brown and Yanagisawa [2] in their investigation of facial nociception in monkeys. The lesions in monkeys B and C involved only parts of the main sensory nucleus and nucleus oralis, and so little can be concluded from the results obtained from these two animals. Perhaps it is worth noting that Carpenter [I] has also reported that partial destruction of the rostra1 part of the trigeminal sensory nuclear complex does not affect facial nociception. In animal D all of the main sensory nucleus on the operated side appeared to have been destroyed, as well as some of the rostra1 part of nucleus oralis, but there did not seem to be any impairment of facial nociception. This finding fits with observations made on four patients in whom it was believed there was destruction of the trigeminal main sensory nucleus on one side as a result of disease. These case histories were originally reported over SO years ago and they have recently been described again in some detail [4]. In each of these cases the patient had a number of neurological abnormalities which included changes in facial sensation: none of the patients had loss of pain or temperature sensibility on the side of the face ipsilateral to the supposed lesion but there were some changes in tactile sensibitity. It was possible to obtain post-mortem confirmation of the supposed lesions in only 2 of the 4 patients. The results from monkey D in these experiments and the information on the effects of lesions in rostra1 trigeminal sensory nuclear complex in man support the view that, from a functional point of view, nociceptor afferents from the face make their principal synaptic connections in the nucleus caudalis of the trigeminal spinal complex. These observations do not support the alternative suggestion on the functional orga~zation of the trigeminal sensory nuclear complex originally proposed by Wall and Taub [12] and again later by Denny-Brown and Yanagisawa f2].
Acknowledgements This project was supported by the M.R.C. I should like to thank Mr. R.J. Chambers and Mr. I.P. Rogers technical assistance and Mrs. M. Clements for secretarial help.
for their skilled
References 1 Carpenter, MB., The dorsal trigeminal tract in the rhesus monkey, .I. Anat. (Lond.), 91 (1957) 82-90. 2 Denny-Brown, D. and Yanagisawa, Y., The function of the descending root of the fifth nerve, Brain, 96 (1973) 783-814. 3 Gerard, M.W., Afferent impulses of the trigeminal nerve, Arch. Neurof. Psychiat. (Chic.), 9 (1923) 306-338.
135 4 Lisney, S.J.W., Destruction of the trigeminal main sensory nucleus and disturbances of facial sensation in man. In: B. Matthews and R.G. Hill (Eds.), Anatomical, Physiological and Pharmacological Aspects of Trigeminal Pain, Excerpta Medica, Amsterdam, 1982, pp. 7-13. 5 Lisney, S.J.W., Some current topics of interest in the physiology of trigeminal pain: a review, J. ray. Sot. Med., 76 (1983) 292-296. 6 Nord, S.G. and Young, R.F., Effects of chronic descending tractotomy on the response patterns of neurons in the trigeminal nuclei principalis and oralis, Exp. Neurol., 65 (1979) 355-372. 7 Olszewski, J., On the anatomical and functional organization of the spinal trigeminal nucleus, J. camp. Neural., 92 (1950) 401-409. 8 Shantha, T.R., Manocha, S.L. and Boume, G.H., A Stereotaxic Atlas of the Java Monkey Brain (Macaca irus), Karger, Basle, 1968. 9 Sjoquist, O., Studies on pain conduction in trigeminal nerve; contribution to surgical treatment of facial pain, Acta psychiat. neurof. stand., Suppl. 17 (1938) l-139. 10 Szabo, J. and Cowan, W.M., A stereotaxic atlas of the brain of the cynomolgus monkey (&fucucu fuscicularis), J. camp. Neurol., 222 (1984) 265-300. 11 Walker, A.E., Anatomy, nerve, J. Neurophysiol., 12 Wall, P.D. and Taub, (1962) 110-126. 13 Young, R.F., Oleson, response to dental pulp
physiology and surgical considerations 2 (1939) 234-248. A., Four aspects of trigeminal nucleus
of the spinal and a paradox,
tract of the trigeminal J. Neurophysiol.,
T.D. and Perryman, K.M., Effect of trigeminaf tractotomy stimuiation in the monkey, J. Neurosurg., 55 (1982) 420-430.
25
on behavioral
Pain, 21 (1985) 129-135 Elsevier
PA1 00712
Observations on Facial Nociception in a Monkey after Destruction of the Rostra1 Part of the Trigeminal Sensory Nuclear Complex S.J.W. Lisney Department of Physiology (Oral Biology), The Medico1 School, University Walk, Bristol BS8 I TD (U.K.) (Received
15 March 1984, accepted
26 September
1984)
Summary Facial sensibility was assessed in a cynomolgus monkey in whom the trigeminal main sensory nucleus and the rostral part of the trigeminal nucleus oralis on one side had been destroyed. The animal responded equally to noxious mechanical stimuli applied to the two sides of the face; no deficiency in nociception could be detected. This finding suggests that the synaptic connections made by nociceptor afferents from the face in rostra1 parts of the trigeminal sensory nuclear complex are not essential for facial nociception. These observations are also consistent with the opinion that, from a functional point of view, facial nociceptor afferents have their principal synaptic connections in the nucleus caudalis of the trigeminal spinal complex.
Introduction In both man and animals, destruction of the caudal part of the trigeminal spinal complex results in a complete or partial loss of pain and temperature sensation on the side of the face ipsilateral to the lesion, with little or no loss of tactile sensibility (for information on man, see refs. 4, 5; on animals, see refs. 2, 3, 6, 11, 13). Those who made the first observations of this sort suggested that the nucleus caudalis was the synaptic station for sensory nerve fibres involved in facial nociception and, since touch and pressure sensibility were preserved, that sensory fibres signalling information about tactile stimulation of the face synapsed with higher order neurones in rostral parts of the trigeminal sensory nuclear complex, particularly the trigeminal 0304-3959/85/%03.30
0 1985 Elsevier Science Publishers
B.V. (Biomedical
Division)
130
main sensory nucleus. This proposal that there were functional subdivisions within the trigeminal sensory nuclear complex became widely accepted and it formed the basis of the rationale behind Sjoquist’s trigeminal tractotomy operation for the relief of persistent trigeminal pain [9]. The clinical results that he and others achieved supported the concept of functional subdivisions within the nuclear complex, and many still hold this view. An alternative view of how the trigeminal sensory nuclear complex may be organized was put forward by Wall and Taub [12], and more recently Denny-Brown and Yanagisawa [2] have taken up this idea and expressed it in more detail. The proposal is that there are no strict functional subdivisions within the complex, but instead the important feature is the neural output of the complex as a whole. For sensations to be perceived. the neural output from the complex to some higher part of the central nervous system has to reach particular critical levels; the critical level of nervous activity needed for pain is higher than that for temperature sensation and this in turn is higher than the level of activity necessary for touch. With this theory the deficiencies in facial sensibility experienced after destruction of the caudal part of the nuclear complex are accounted for in terms of loss of output from the complex as a whole following damage to part of it rather than in terms of destruction of a specific set of synaptic connections. If this view is correct, one would expect localized destruction of some other part of the nuclear complex to result in an ipsilateral loss of pain sensibility but if the more established view is correct, such a lesion should leave facial pain sensibility unaltered. The experiments described here were carried out to see which of these two possibilities occurred following localized lesions in rostra1 parts of the trigeminal sensory nuclear complex.
Methods
Six feral, male cynomolgus monkeys (Mucaca f~cjcu~arj~} weighing between 3.5 and 5.5 kg were used in the experiments. Over a period of several months they were trained to leave their cages and sit in a restraint chair where they were introduced to the procedures that later would be used to test facial sensibility. The method used was based on that described by Denny-Brown and Yanagisawa [2] in their study of facial nociception in monkeys; additional practical advice was obtained from correspondence with Dr. Denny-Brown. It involved stimulating the face and head by stroking and pressing the skin with a blunt ended plastic rod, displacing a few hairs with the rod, and pricking and scratching with a pin fixed into the end of a second, similar rod. A movement of the animal, whether the movement was of the whole head away from the source of the stimulus or just a slight movement of the facial musculature, was taken as an indication that the animal had perceived the stimulus. Occasionally the animals would make threatening gestures, baring their teeth, for example, in response to noxious stimuli. Both sides of the head and face were tested so that responses following stim~ation on the experimental side could be compared with those to the same stimulus on the normal side. None of the animals would allow testing in or around the mouth and the design of the restraint chair was such
131
that skin under the chin and lower jaw could not be tested satisfactorily. Each testing session lasted 25-35 min, during which rewards of fruit were given periodically. One animal did not tolerate these procedures and it had to be eliminated from the project. Once the monkeys were accustomed to facial sensibility testing, a brief operation was carried out in which stereotaxic, electrolytic lesions were made in rostra1 parts of the left t~ge~nal sensory nuclear complex. The animals were anaesthetized with ketamine hydrochloride (20 mg/kg i.m.) followed by sodium pentobarbitone (24 mg/kg i.p.) and then placed in a Kopf stereotaxic frame. The scalp and temporalis muscle on the left side were reflected, a small hole made in the cranium at the appropriate place, and the lesioning electrode positioned in the trigeminal main sensory nucleus and/or the nucleus oralis of the spinal trigeminal complex (Olszewski’s terminology [7]), using stereotaxic coordinates from the atlas of Shantha et al. (81. Lesions were made by passing DC current (5 mA, 30 set) between the tip of the electrode (anode) and an indifferent electrode attached to a saline soaked pad on the exposed temporalis muscle. Lesions were made at several adjacent sites in each animal. The muscle and skin wounds were sutured separately, an intramuscular injection of penicillin given and then the animals were allowed to recover. Testing of facial sensation began again 4-7 days after the operation and continued several times a week for 4-6 weeks. At the end of this period the animals were re-anaesthetized and perfused via both carotid arteries with 1 litre of Ringer’s solution with 1% procaine as a pre-wash followed by 3 litres of phosphate-buffered formaldehyde fixative. Each brain was left in fixative for a further 1 or 2 weeks and then 80 pm serial, frozen sections were cut from the brain-stem for histological identification of the lesion sites.
Because of variation in brain size from animal to animal, it is difficult to make stereotaxic lesions with pin-point accuracy [lo]. In 2 of the 5 animals the lesions produced were misplaced, in 2 animals the lesions destroyed only parts of the trigeminal main sensory nucleus or the nucleus orahs, and in 1 animal the main sensory nucleus and the rostra1 part of nucleus oralis appeared to be completely destroyed. The positions of the lesions in these last 3 monkeys are shown in Fig. 1. Animal D was the one in which all the main sensory nucleus and some of the rostral part of nucleus oralis were destroyed; most of the trigeminal descending spinal tract was spared, being just lateral to the lesion, but some of the medial part was damaged. Parts of the trigeminal motor nucleus and the nucleus of the facial nerve were also involved in the lesion; this was anticipated as there was wasting of the temporalis and masseter muscles and paralysis of some of the facial muscles on the lesioned side. The lesion extended more dorsally than planned, involving cerebellar pathways, and the animal showed some locomotor disability as a consequence. Despite these complications, the animal ate normally, it learned to cope with its lack of motor coordination and it continued to cooperate in the experiment.
132 ANIMAL
8
._ _j L ,‘OI. (’
ANIMAL
C
ANIMAL
0
2’
PY ; ’
-10 8
6
4
2
0
8
6
4
2
0
\
-10
Y--
5
imml
0
133
Testing of facial sensibility in monkey D failed to reveal any difference in the response to noxious mechanical stimulation (pin-prick, pin-scratch) between the normal and operated sides of the face. The usual response to a noxious stimulus was a brisk turning of the head away from the direction of stimulation; occasionally the animal would frown, as if in disapproval, or make a threatening gesture. Alarm calls were not made. These responses were not observed when the blunt plastic rod was used to apply non-noxious mechanical stimuli to the same areas of the face and so it seems unlikely that visual clues were important in eliciting these responses. The same results were obtained with the 2 animals, monkeys B and C, in which there was only partial destruction of the rostra1 part of the trigeminal sensory nuclear complex. It was more difficult to make decisions about responses to non-noxious stimulation of the face. Before their operation all the animals had become accustomed to having their faces and heads stroked, touched and pressed by a blunt plastic rod and they seemed to be indifferent to this type of stimulation. If, however, just a few of the longer guard hairs were displaced, the animals would occasionally respond with a slight jerk of the head or a twitch of an adjacent facial muscle. The impression gained was that this type of light, tactile stimulation was irritating, like a fly walking across the skin. After the lesion operations the animals showed the same indifference to touch and light pressure but in animals B and D, where there was some paralysis of the facial musculature, it was more difficult to detect responses to movements of guard hairs.
Discussion
From the outset it must be said that although the methods used to test facial sensation were essentially those used in clinical neurological examinations, they are relatively crude and can only give an impression of facial sensibility. This is particularly so when used with animals, where the investigator has to make an assessment on the evidence of outward signs alone and the subject cannot give additional verbal information. It may well be that there were subtle changes in facial
-~
--.
Fig. 1. Diagrams showing the positions of the lesions in monkeys B, C and D. On the right are dorsal views of the brain-stem showing the antero-posterior position of each lesion in relation to the Horsley-Clark stereotaxic coordinates; the diagrams were drawn using information from the atlases of Shantha et al. [8] and Szabo and Cowan [lo]. The stippling shows the positions of the trigeminal main sensory nucleus and the trigeminal spinal complex. Olszewski [7] states that in the trigeminal spinal complex, the transition from the nucleus interpolar6 to the nucleus oralis takes place at the level of the oral third of the inferior olive; in this diagram this would be between AP -0.5 and iO.5. In each diagram the cross-hatching indicates the extent of the lesion. On the left are drawings made from coronal sections of the brain-stem showing the individual lesion sites at the AP levels indicated by the arrows. Abbreviations (using the nomenclature of Shantha et al. [8]): BC, bra&urn conjunctivum; DR, nucleus dorsalis raphe; NF, nucleus n. facialis; NMA, nucleus medialis anuli aquaeducti; NMV, nucleus motorius n. trigemini; NW, nucleus tractus spinalis n. trigemini; 01, nucleus olivaris inferior; PVA, nucleus principalis n. trigeminalis; PY, tractus pyrimidalis; TSV, tractus spinalis n. trigemini.
134
sensation in these lesioned animals that went undetected. Although it would have been possible to devise more sophisticated methods of testing facial sensibility, it was decided to use these more simple procedures so that the results obtained would be directly comparable with those obtained by Denny-Brown and Yanagisawa [2] in their investigation of facial nociception in monkeys. The lesions in monkeys B and C involved only parts of the main sensory nucleus and nucleus oralis, and so little can be concluded from the results obtained from these two animals. Perhaps it is worth noting that Carpenter [I] has also reported that partial destruction of the rostra1 part of the trigeminal sensory nuclear complex does not affect facial nociception. In animal D all of the main sensory nucleus on the operated side appeared to have been destroyed, as well as some of the rostra1 part of nucleus oralis, but there did not seem to be any impairment of facial nociception. This finding fits with observations made on four patients in whom it was believed there was destruction of the trigeminal main sensory nucleus on one side as a result of disease. These case histories were originally reported over SO years ago and they have recently been described again in some detail [4]. In each of these cases the patient had a number of neurological abnormalities which included changes in facial sensation: none of the patients had loss of pain or temperature sensibility on the side of the face ipsilateral to the supposed lesion but there were some changes in tactile sensibitity. It was possible to obtain post-mortem confirmation of the supposed lesions in only 2 of the 4 patients. The results from monkey D in these experiments and the information on the effects of lesions in rostra1 trigeminal sensory nuclear complex in man support the view that, from a functional point of view, nociceptor afferents from the face make their principal synaptic connections in the nucleus caudalis of the trigeminal spinal complex. These observations do not support the alternative suggestion on the functional orga~zation of the trigeminal sensory nuclear complex originally proposed by Wall and Taub [12] and again later by Denny-Brown and Yanagisawa f2].
Acknowledgements This project was supported by the M.R.C. I should like to thank Mr. R.J. Chambers and Mr. I.P. Rogers technical assistance and Mrs. M. Clements for secretarial help.
for their skilled
References 1 Carpenter, MB., The dorsal trigeminal tract in the rhesus monkey, .I. Anat. (Lond.), 91 (1957) 82-90. 2 Denny-Brown, D. and Yanagisawa, Y., The function of the descending root of the fifth nerve, Brain, 96 (1973) 783-814. 3 Gerard, M.W., Afferent impulses of the trigeminal nerve, Arch. Neurof. Psychiat. (Chic.), 9 (1923) 306-338.
135 4 Lisney, S.J.W., Destruction of the trigeminal main sensory nucleus and disturbances of facial sensation in man. In: B. Matthews and R.G. Hill (Eds.), Anatomical, Physiological and Pharmacological Aspects of Trigeminal Pain, Excerpta Medica, Amsterdam, 1982, pp. 7-13. 5 Lisney, S.J.W., Some current topics of interest in the physiology of trigeminal pain: a review, J. ray. Sot. Med., 76 (1983) 292-296. 6 Nord, S.G. and Young, R.F., Effects of chronic descending tractotomy on the response patterns of neurons in the trigeminal nuclei principalis and oralis, Exp. Neurol., 65 (1979) 355-372. 7 Olszewski, J., On the anatomical and functional organization of the spinal trigeminal nucleus, J. camp. Neural., 92 (1950) 401-409. 8 Shantha, T.R., Manocha, S.L. and Boume, G.H., A Stereotaxic Atlas of the Java Monkey Brain (Macaca irus), Karger, Basle, 1968. 9 Sjoquist, O., Studies on pain conduction in trigeminal nerve; contribution to surgical treatment of facial pain, Acta psychiat. neurof. stand., Suppl. 17 (1938) l-139. 10 Szabo, J. and Cowan, W.M., A stereotaxic atlas of the brain of the cynomolgus monkey (&fucucu fuscicularis), J. camp. Neurol., 222 (1984) 265-300. 11 Walker, A.E., Anatomy, nerve, J. Neurophysiol., 12 Wall, P.D. and Taub, (1962) 110-126. 13 Young, R.F., Oleson, response to dental pulp
physiology and surgical considerations 2 (1939) 234-248. A., Four aspects of trigeminal nucleus
of the spinal and a paradox,
tract of the trigeminal J. Neurophysiol.,
T.D. and Perryman, K.M., Effect of trigeminaf tractotomy stimuiation in the monkey, J. Neurosurg., 55 (1982) 420-430.
25
on behavioral