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Postsynaptic fibres in the dorsal columns and their relay in the nucleus gracilis
380
SHORT COMMUNICATIONS
Postsynaptic fibres in the dorsal columns and their relay in the nucleus gracilis The fasciculus gracilis contains primary afferent fibres which have their somata in dorsal root ganglia and innervate the hindlimb, trunk and tail. Some of these fibres extend rostrally to the nucleus gracilis and others leave the dorsal columns at lumbar and thoracic levels6. Those fibres which reach the nucleus gracilis are generally assumed to mediate information from low threshold cutaneous mechanoreceptors and from certain receptors in deeper structures 11. Recent experiments have shown that the fasciculus gracilis is surprisingly selective toward the primary afferent fibres it conveys rostrally: large afferent fibres supplying certain low threshold cutaneous mechanoreceptors do not extend to cervical levels in this pathway 9, nor do fibres supplying most hindlimb articular receptors 3. In addition to primary afferent neurones, Petit et al. ~o have identified postsynaptic fibres in the fasciculus gracilis which resemble those described by Uddenberg in the cuneate tract 14. They showed convergent properties that in the present study have been compared with the properties of a population of relay cells in the nucleus gracilis. Cats were anaesthetized either with Nembutal or chloraiose; the activities of single units were recorded from the fasciculus gracilis (fibres) at the thoracic level (Th 12) and from the nucleus gracilis (cells), using micropipettes or tungsten microelectrodes. Usual criteria were used to distinguish the activity of a fibre from that of a cell (the duration of the spike, its polarity, the absence or presence of injury discharge). As the microelectrode was advanced through the structure, the sciatic nerve was electrically stimulated at a strength that was supramaximal for the myelinated fibres. Several stimulations were applied for examination of receptive field properties: hair movements and light pressure were given by a hand held glass rod with a fire polished tip 3 mm in diameter; three clips were used to grasp a fold of skin and provide 3 constant stimuli that were roughly called: non-noxious, firm and noxious, according to the reactions of a freely moving cat; heating of the skin was performed with a radiant source or with a contact heating device; cooling was achieved by evaporation of ether, this last thermal stimulus being an innocuous one. (1) Thoracic level. The 3 following criteria were utilized to distinguish the postsynaptic activity from a primary afferent response associated with a dorsal root reflexZ,~5: (a) a single shock to the sciatic nerve elicited a high frequency multiple discharge (6 or 8 impulses); (b) with the repetition of a threshold electrical stimulus, the latency of the response fluctuated (up to 0.4 or 0.5 msec); (c) the rate of frequency following did not exceed 200/sec even for the first spike of the discharge. 137 fibres, i.e. 14.5~,, of the fibres activated from cutaneous receptive fields or 9.3 % of the total number of fibres seen at the thoracic level, fulfilled these requirements and were classified as postsynaptic fibres. All but a few of the postsynaptic fibres studied in the fasciculus gracilis at Th 12 reached upper cervical levels. They lay within 500-1000 #m from the surface of the spinal cord. When classified according to their responses to natural stimulation s, 77 % of the units examined showed convergent properties, receiving inputs from several Brain Research, 48 (1972) 380-384
SHORT COMMUNICATIONS
381
Fig. 1. Responsesevoked in a postsynaptic fibre of the fasciculusgracilis by mechanicalstimulations (lines below the recordings). A, Responses to several successivehair movements. B, C and D, Responses to the application of the non-noxious(B),firm (C) or noxious (D) clip (constant stimulations).
different receptor types. Most fibres of this group had an irregular low frequency background activity of 2-4/see. They were activated by hair movement (rapidly adapting discharge) and gave a slowly adapting response to constant skin distorsion: gentle pressure or strong pinching (Fig. 1). The frequency of the evoked tonic discharge increased according to the strength of the applied mechanical stimulus, even when it was brought well into the noxious range. It reached 150 or 200/sec when the noxious clip was applied and the intervals between two successive spikes were as short as 1 msec. Noxious heating of the skin with radiant heat produced a vigorous discharge (up to 300/sec). Contact heating produced a slowly adapting discharge which occurred when the skin surface temperature exceeded 45 °C. Rapid cooling of the skin by ether evaporation elicited a discharge, the frequency of which was usually lower than that obtained with noxious stimulation. The size of the receptive fields varied with their location on the limb, the more distal being the smaller ones. The sensitivity inside the field was uneven and many of the low threshold points of sensitivity were type I 'dome' receptors first described by Iggo 5. In addition, electrical stimulation of group III muscle fibres that innervate 'pressure-pain' receptors1, 7 seemed to activate some of these units. This has been confirmed by natural stimulation of the muscle, on which light pressure was effective to elicit a response. (2) Bulbar level. At the bulbar level, most of the recordings were obtained in the middle part (see ref. 4) of the nucleus gracilis. The cells tested with natural stimulations (134 units) have been classified into 3 groups. One type of cell was activated by hair movement and the responses were rapidly adapting. The cells of the second group responded to gentle or brisk tapping. These results are in agreement with data obtained by previous workers4, s. The units of the third group (30 ~o) did not differ from the former ones as far as the properties of their responses to electrical stimulation of the sciatic nerve (number of spikes, latency, fatigability) and the depth of their location (most of them were Brain Research, 48 (1972) 380-384
5'
Fig. 2. Responses of a unit of the nucleus gracilis showing a high degree of modality convergence. A, Responses to hair movements. B, C and D, Responses to the application of the non-noxious (B), firm (C) or noxious (D) clip.
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383
situated between 800 and 1500/~m from the surface) are considered; but they showed a high degree of modality convergence that contrasted with the specific properties of the previous two groups of neurones. They responded to hair movement, to light pressure on the skin, strong pressure and pinching. A steady mechanical stimulus elicited a sustained discharge (Fig. 2) the frequency of which incremented with the strength of the stimulation, but it never exceeded 50/sec. Except for one case that did not respond and for two cases in which the activation followed a short period of complete inhibition of the background discharges, all the cells of this group that were tested with noxious radiant heat responded to this stimulus. The frequency of the discharge evoked by such a thermal stimulation was usually lower than the frequency of the response elicited by mechanical stimulation. All of these cells were activated by cooling. After a lesion of the whole spinal cord but the dorsal columns, at the thoracic level, such convergent responses were still recorded from single cells in th6 nucleus. The striking features of these gracilis units are their modality convergence, and their responsiveness to noxious mechanical and thermal stimuli. One of the common properties they have with the dorsal columns postsynaptic fibres is that C fibres contribute to their activity, as judged from their response to noxious heat. However, it is known that C primary afferent fibres do not ascend the fasciculus gracilis 18. A possible explanation of the properties of these cells is that some neurones in the nucleus gracilis receive information conveyed by the postsynaptic fibres of the dorsal columns, but the high ratio of cells contrasting with the low proportion of fibres of this type implies considerable branching of the ascending fibres at the bulbar level. Supporting this interpretation is the recent anatomical data from Rustioni 12 in which non-primary afferents from lumbar dorsal columns are shown to reach the nucleus gracilis. Whether such fibres terminate at the bulbar level or activate the gracilis cells through collaterals while ascending further rostrally is still unknown. I wish to express my gratitude to Dr. P. R. Burgess for highly helpful discussion and to Mrs. E. Boudinot for skilful technical assistance. Centre d'Etudes de Physiologie nerveuse du CNRS, 75016 Paris (France)
DENISE PETIT*
1 BEssou, P., ET LAPORTE, Y., Etude des r6cepteurs musculaires innerv6s par les fibres aff6rentes du groupe III (fibres my~,linis6esfines) chez le Chat, Arch. ital. Biol., 99 (1961) 293-321. 2 BROOKS,C. C., AND KOmUMI, K., Origin of the dorsal root reflex, J. Neurophysiol., 19 (1956) 61-74. 3 BURGESS, P. R., AND CLARK, F. J., Dorsal column projection of fibres from the cat knee joint, J. Physiol. (Lond.), 203 (1969) 301-315. 4 GORDON,G., AND JUKES,M. G. M., Dual organization of the exteroceptive components of the cat's gracile nucleus, J. Physiol. (Lond.), 173 (1964) 263-290. * Present address: D6partement de Psychophysiologie g6n6rale, Institut de Neurophysiologie et Psychophysiologie, C.N.R.S., 31, chemin Joseph Aiguier, 13274 Marseille Cedex 2, France. Brain Research, 48 (1972) 380-384
384
SHORT COMMUNICATIONS
5 IGGO, A., New specific sensory structures in hairy skin, Acta Neuroveg. (Wien), 24 (1963) 175-180. 6 LLOYD, D. P. C., AND MclNTYRE, A. K., Dorsal column conduction of group I muscle afferent impulses and their relay through Clarke's column, J. Neurophysiol., 13 (1950) 39-54. 7 PAINTAL,A. S., Functional analysis of group III afferent fibres of mammalian muscles, J. Physiol. (Lond.), 152 (1960) 250-270. 8 PERL, E. R., WHITLOCK,D. G., AND GENTRY, J. R., Cutaneous projection to second order neurons of the dorsal column system, J. Neurophysiol., 25 (1962) 337-358. 9 PETIT, D., AND BURGESS,P. R., Dorsal column projection of receptors in cat hairy skin supplied by myelinated fibers, J. Neurophysiol., 31 (1968) 849-855. 10 PETIT, D., LACKNER, D., ET BURGESS,P. R., Mise en 6vidence de fibres "hactivit6 post-synaptique au niveau des colonnes dorsales chez le Chat, J. Physiol. (Paris), 61 (1969) 372-373. 11 ROSE, J. E., AND MOUNTCASTLE,V. B., Touch and Kinesthesis. In J. FIELD, H. W. MAGOUNAND V. E. HALL (Eds.), Handbook of Physiology, Sect. 1, Neurophysiology, Vol. 1, Amer. Physiol. Soc., Washington, 1959, pp. 387-430. 12 RUSTIONI, A., Non-primary afferents to the nucleus gracilis from the lumbar cord of the cat, Brain Research, in press. 13 SZENTAGOTHAI,J., Neuronal and synaptic arrangement in the substantia gelatinosa Rolandi, J. comp. Neurol., 122 (1964) 219-240. 14 UDDENBERG,N., Functional organization of long, second order afferents in the dorsal funiculus, Exp. Brain Res., 4 (1968) 377-382. 15 WALL,P. D., Repetitive discharge of neurons, J. Neurophysiol., 22 (1959) 305-320. (Accepted August 24th, 1972)
Brain Research, 48 (1972) 380--384
SHORT COMMUNICATIONS
Postsynaptic fibres in the dorsal columns and their relay in the nucleus gracilis The fasciculus gracilis contains primary afferent fibres which have their somata in dorsal root ganglia and innervate the hindlimb, trunk and tail. Some of these fibres extend rostrally to the nucleus gracilis and others leave the dorsal columns at lumbar and thoracic levels6. Those fibres which reach the nucleus gracilis are generally assumed to mediate information from low threshold cutaneous mechanoreceptors and from certain receptors in deeper structures 11. Recent experiments have shown that the fasciculus gracilis is surprisingly selective toward the primary afferent fibres it conveys rostrally: large afferent fibres supplying certain low threshold cutaneous mechanoreceptors do not extend to cervical levels in this pathway 9, nor do fibres supplying most hindlimb articular receptors 3. In addition to primary afferent neurones, Petit et al. ~o have identified postsynaptic fibres in the fasciculus gracilis which resemble those described by Uddenberg in the cuneate tract 14. They showed convergent properties that in the present study have been compared with the properties of a population of relay cells in the nucleus gracilis. Cats were anaesthetized either with Nembutal or chloraiose; the activities of single units were recorded from the fasciculus gracilis (fibres) at the thoracic level (Th 12) and from the nucleus gracilis (cells), using micropipettes or tungsten microelectrodes. Usual criteria were used to distinguish the activity of a fibre from that of a cell (the duration of the spike, its polarity, the absence or presence of injury discharge). As the microelectrode was advanced through the structure, the sciatic nerve was electrically stimulated at a strength that was supramaximal for the myelinated fibres. Several stimulations were applied for examination of receptive field properties: hair movements and light pressure were given by a hand held glass rod with a fire polished tip 3 mm in diameter; three clips were used to grasp a fold of skin and provide 3 constant stimuli that were roughly called: non-noxious, firm and noxious, according to the reactions of a freely moving cat; heating of the skin was performed with a radiant source or with a contact heating device; cooling was achieved by evaporation of ether, this last thermal stimulus being an innocuous one. (1) Thoracic level. The 3 following criteria were utilized to distinguish the postsynaptic activity from a primary afferent response associated with a dorsal root reflexZ,~5: (a) a single shock to the sciatic nerve elicited a high frequency multiple discharge (6 or 8 impulses); (b) with the repetition of a threshold electrical stimulus, the latency of the response fluctuated (up to 0.4 or 0.5 msec); (c) the rate of frequency following did not exceed 200/sec even for the first spike of the discharge. 137 fibres, i.e. 14.5~,, of the fibres activated from cutaneous receptive fields or 9.3 % of the total number of fibres seen at the thoracic level, fulfilled these requirements and were classified as postsynaptic fibres. All but a few of the postsynaptic fibres studied in the fasciculus gracilis at Th 12 reached upper cervical levels. They lay within 500-1000 #m from the surface of the spinal cord. When classified according to their responses to natural stimulation s, 77 % of the units examined showed convergent properties, receiving inputs from several Brain Research, 48 (1972) 380-384
SHORT COMMUNICATIONS
381
Fig. 1. Responsesevoked in a postsynaptic fibre of the fasciculusgracilis by mechanicalstimulations (lines below the recordings). A, Responses to several successivehair movements. B, C and D, Responses to the application of the non-noxious(B),firm (C) or noxious (D) clip (constant stimulations).
different receptor types. Most fibres of this group had an irregular low frequency background activity of 2-4/see. They were activated by hair movement (rapidly adapting discharge) and gave a slowly adapting response to constant skin distorsion: gentle pressure or strong pinching (Fig. 1). The frequency of the evoked tonic discharge increased according to the strength of the applied mechanical stimulus, even when it was brought well into the noxious range. It reached 150 or 200/sec when the noxious clip was applied and the intervals between two successive spikes were as short as 1 msec. Noxious heating of the skin with radiant heat produced a vigorous discharge (up to 300/sec). Contact heating produced a slowly adapting discharge which occurred when the skin surface temperature exceeded 45 °C. Rapid cooling of the skin by ether evaporation elicited a discharge, the frequency of which was usually lower than that obtained with noxious stimulation. The size of the receptive fields varied with their location on the limb, the more distal being the smaller ones. The sensitivity inside the field was uneven and many of the low threshold points of sensitivity were type I 'dome' receptors first described by Iggo 5. In addition, electrical stimulation of group III muscle fibres that innervate 'pressure-pain' receptors1, 7 seemed to activate some of these units. This has been confirmed by natural stimulation of the muscle, on which light pressure was effective to elicit a response. (2) Bulbar level. At the bulbar level, most of the recordings were obtained in the middle part (see ref. 4) of the nucleus gracilis. The cells tested with natural stimulations (134 units) have been classified into 3 groups. One type of cell was activated by hair movement and the responses were rapidly adapting. The cells of the second group responded to gentle or brisk tapping. These results are in agreement with data obtained by previous workers4, s. The units of the third group (30 ~o) did not differ from the former ones as far as the properties of their responses to electrical stimulation of the sciatic nerve (number of spikes, latency, fatigability) and the depth of their location (most of them were Brain Research, 48 (1972) 380-384
5'
Fig. 2. Responses of a unit of the nucleus gracilis showing a high degree of modality convergence. A, Responses to hair movements. B, C and D, Responses to the application of the non-noxious (B), firm (C) or noxious (D) clip.
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©
©
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SHORT COMMUNICATIONS
383
situated between 800 and 1500/~m from the surface) are considered; but they showed a high degree of modality convergence that contrasted with the specific properties of the previous two groups of neurones. They responded to hair movement, to light pressure on the skin, strong pressure and pinching. A steady mechanical stimulus elicited a sustained discharge (Fig. 2) the frequency of which incremented with the strength of the stimulation, but it never exceeded 50/sec. Except for one case that did not respond and for two cases in which the activation followed a short period of complete inhibition of the background discharges, all the cells of this group that were tested with noxious radiant heat responded to this stimulus. The frequency of the discharge evoked by such a thermal stimulation was usually lower than the frequency of the response elicited by mechanical stimulation. All of these cells were activated by cooling. After a lesion of the whole spinal cord but the dorsal columns, at the thoracic level, such convergent responses were still recorded from single cells in th6 nucleus. The striking features of these gracilis units are their modality convergence, and their responsiveness to noxious mechanical and thermal stimuli. One of the common properties they have with the dorsal columns postsynaptic fibres is that C fibres contribute to their activity, as judged from their response to noxious heat. However, it is known that C primary afferent fibres do not ascend the fasciculus gracilis 18. A possible explanation of the properties of these cells is that some neurones in the nucleus gracilis receive information conveyed by the postsynaptic fibres of the dorsal columns, but the high ratio of cells contrasting with the low proportion of fibres of this type implies considerable branching of the ascending fibres at the bulbar level. Supporting this interpretation is the recent anatomical data from Rustioni 12 in which non-primary afferents from lumbar dorsal columns are shown to reach the nucleus gracilis. Whether such fibres terminate at the bulbar level or activate the gracilis cells through collaterals while ascending further rostrally is still unknown. I wish to express my gratitude to Dr. P. R. Burgess for highly helpful discussion and to Mrs. E. Boudinot for skilful technical assistance. Centre d'Etudes de Physiologie nerveuse du CNRS, 75016 Paris (France)
DENISE PETIT*
1 BEssou, P., ET LAPORTE, Y., Etude des r6cepteurs musculaires innerv6s par les fibres aff6rentes du groupe III (fibres my~,linis6esfines) chez le Chat, Arch. ital. Biol., 99 (1961) 293-321. 2 BROOKS,C. C., AND KOmUMI, K., Origin of the dorsal root reflex, J. Neurophysiol., 19 (1956) 61-74. 3 BURGESS, P. R., AND CLARK, F. J., Dorsal column projection of fibres from the cat knee joint, J. Physiol. (Lond.), 203 (1969) 301-315. 4 GORDON,G., AND JUKES,M. G. M., Dual organization of the exteroceptive components of the cat's gracile nucleus, J. Physiol. (Lond.), 173 (1964) 263-290. * Present address: D6partement de Psychophysiologie g6n6rale, Institut de Neurophysiologie et Psychophysiologie, C.N.R.S., 31, chemin Joseph Aiguier, 13274 Marseille Cedex 2, France. Brain Research, 48 (1972) 380-384
384
SHORT COMMUNICATIONS
5 IGGO, A., New specific sensory structures in hairy skin, Acta Neuroveg. (Wien), 24 (1963) 175-180. 6 LLOYD, D. P. C., AND MclNTYRE, A. K., Dorsal column conduction of group I muscle afferent impulses and their relay through Clarke's column, J. Neurophysiol., 13 (1950) 39-54. 7 PAINTAL,A. S., Functional analysis of group III afferent fibres of mammalian muscles, J. Physiol. (Lond.), 152 (1960) 250-270. 8 PERL, E. R., WHITLOCK,D. G., AND GENTRY, J. R., Cutaneous projection to second order neurons of the dorsal column system, J. Neurophysiol., 25 (1962) 337-358. 9 PETIT, D., AND BURGESS,P. R., Dorsal column projection of receptors in cat hairy skin supplied by myelinated fibers, J. Neurophysiol., 31 (1968) 849-855. 10 PETIT, D., LACKNER, D., ET BURGESS,P. R., Mise en 6vidence de fibres "hactivit6 post-synaptique au niveau des colonnes dorsales chez le Chat, J. Physiol. (Paris), 61 (1969) 372-373. 11 ROSE, J. E., AND MOUNTCASTLE,V. B., Touch and Kinesthesis. In J. FIELD, H. W. MAGOUNAND V. E. HALL (Eds.), Handbook of Physiology, Sect. 1, Neurophysiology, Vol. 1, Amer. Physiol. Soc., Washington, 1959, pp. 387-430. 12 RUSTIONI, A., Non-primary afferents to the nucleus gracilis from the lumbar cord of the cat, Brain Research, in press. 13 SZENTAGOTHAI,J., Neuronal and synaptic arrangement in the substantia gelatinosa Rolandi, J. comp. Neurol., 122 (1964) 219-240. 14 UDDENBERG,N., Functional organization of long, second order afferents in the dorsal funiculus, Exp. Brain Res., 4 (1968) 377-382. 15 WALL,P. D., Repetitive discharge of neurons, J. Neurophysiol., 22 (1959) 305-320. (Accepted August 24th, 1972)
Brain Research, 48 (1972) 380--384