Brain Research, 98 (1975) 359-363 © ElsevierScientificPublishingCompany,Amsterdam- Printed in The Netherlands
359
Does the spinocervical pathway exist?
S. A. A N D E R S S O N AND P. E. L E I S S N E R
Department of Physiology, University of Grteborg, Giiteborg 33 (Sweden)
(Accepted July 7th, 1975)
The existence of cortical responses of short latency to afferent volleys travelling in the dorsolateral funiculus of the spinal cord has been pointed out in many investigations1,2,5-9. Studies after selective lesions of the spinal cord at different levels have indicated that a synchronous volley ascending via the spinocervico-lemniscal pathway elicits a prominent positive-negative surface potential in the cortical areas SI and SII, with the same or shorter latency as that of an afferent volley mediated via the dorsal column. Single cortical units were also found to be excited with short latency from small contralateral receptive fields after lesions, leaving intact only the spinocervicolemniscal pathway1,4. Some authors3,10, using a method of direct electrical stimulation of the spinal cord, were not able to verify these effects. Instead, they found only a small positive or negative surface response in the somatosensory cortex after electrical stimulation of the dorsolateral funiculus at the cervical level of the spinal cord, when spread of current to the dorsal column was prevented by a mica plate inserted between the dorsal column and the lateral funiculus. After a lesion of the dorsal columns only few wide-field cortical neurones were influenced by peripheral adequate stimulation. These authors suggested that the short latency positive-negative potentials and the activation of cortical cells from small receptive fields, described by the previous investigators as due to activity in a pathway in the dorsolateral funiculus, in fact should be related to incomplete lesions of the dorsal columns and/or elimination of tonic interaction between two pathways. The present study was undertaken to elucidate this controversy by repeating the experiments of Towe and coworkers using a slight modification of their technique in order to minimize the damage to the dorsal horn and to fibres ascending in the dorsolateral funiculus. Two cats weighing 2.6 and 3.3 kg respectively were anaesthetized with 50 mg chloralose/kg i.p. and immobilized with decamethonium bromide i.v. Artificial respiration was given and the end-tidal pCOz was maintained at 4.5 ~. The body temperature was kept at 38 °C. Both cerebral hemispheres were exposed and the dorsal laminae of vertebrae Cz, C4 and C5 were removed. After opening the dura mater, the brain and the spinal cord were covered with warm mineral oil. An incision was made on one side in the pia mater along the dorsal root entry zone from mid C4 to mid C5. The dorsal column was then separated from the inner surface of the dorsal horn down
360 I
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500 MA
I000 IAA
~
[ 1,300 pV rostr
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, .-.,_./ C
I [ I00 ~JV
I ~ X ~
5 mse¢ 25 msec
/
B
[ 400 pV
D 500 ~A J
HOOOpA
400 [JV
5 msec dorso~at funiculus stim.
Fig. 1. Arrangement of the stimulation electrodes and the appearance of the responses recorded from the somatosensory cortex at the indicated stimulation intensities applied to the contralateral cervical spinal cord. Stimulation at the dorsal column at the level of the insulating sheet (A) and at a more rostral location (B). Note the shorter latency in B. Stimulation of the dorsolateral funiculus at the level of the insulating sheet (C) and at a more rostral location (D). Note the notch in the initial positivity in D. E: Superimposed traces, showing the average responses of 16 consecutive stimulations of the dorsolateral funiculus and of the dorsal column respectively at the level of the insulating sheet and of the same stimulation intensity, 1000/~A. In all traces positivity is downwards. to the central canal leaving the blood vessels intact as much as possible. The dorsal column was tilted with the aid o f blunt glass hooks and a 0.2 m m × 15 m m x 15 mm teflon sheet was inserted under visual control between the dorsal column and the dorsolateral funiculus down to the central canal. Electrical stimulation could be delivered to pairs o f ball tipped A g - A g C I electrodes with an interelectrode distance o f 2.5 m m placed over the dorsal column and the dorsolateral funiculus, on either side as well as just rostral or caudal to the insulating teflon sheet (Fig. 1). Peripheral stimulation was carried out via pairs of needles, inserted in the central pads o f the fore- and hindpaws bilaterally. Stimulation was performed with 0.2 msec square pulses. The evoked cortical surface potentials were recorded via ball tipped A g - A g C I electrodes and fed into a conventional amplifying equipment with a low frequency cutoff(--3 dB) at l H z and a high frequency cutoff at 30 k H z and displayed on a CRO. Consecutive responses could be averaged on a Hewlett Packard, model 5480A. At the end o f the experiment the spinal cord was fixed in situ with 10 ~ formalin. The surgical interference with the dorsal column and the dorsolateral funiculus was examined microscopically in 50 # m frozen sections o f the spinal cord. Fig. 1 illustrates the arrangement o f the stimulating electrodes and the surface potentials evoked in the contralateral somatosensory area I. Electrical stimulation o f the dorsal columns caudal, medial or rostral to the insulating sheet (Fig. I A and B) elicited a positive-negative response in a large area o f the somatosensory cortex. The threshold response was obtained at an intensity o f about 50 #A. At stimulation intensities of more than two times the threshold, the characteristics and the distribution o f the cortical response remained virtually unchanged at different placements of the
361 stimulating electrodes on the contralateral dorsal co'.umn. The amplitude increased at higher stimulation intensities and could reach 1.5 mV at a stimulation strength of 0.5 mA. At low stimulation intensities the onset latency of the cortical response was about 5.5 msec, but the latency decreased to about 4.5 msec when a stimulation of high intensity, usually more than 5 times threshold, was applied to the dorsal columns rostral or caudal to the insulating sheet (Fig. 1B). No such shortening of the latency was found at stimulation of the dorsal columns at the level of the insulating sheet (Fig. 1A). Stimulation of the dorsolateral funiculus also elicited a positive-negative response at a similar intensity as stimulation of the dorsal column (Fig. 1C and D). The amplitude was about one third of that obtained with a corresponding stimulation intensity applied to the dorsal columns. The onset latency of the cortical response was about 4.5 msec and thus similar to the latency of the response elicited by high intensity stimulation of the dorsal column rostral to the insulating sheet. The characteristics and latencies of the cortical responses remained unchanged at increasing intensity of a stimulus applied to the lateral funiculus at the level of the insulating sheet. Stimulation of the dorsolateral funiculus with high intensities (1 mA) at sites caudal or rostral to the insulating sheet gave a notch (arrow) in the initial potential (Fig. 1D). Although the onset latency was the same as at lower stimulation intensities a second positivity appeared in the response at a latency similar to that of the positive potentials evoked via the dorsal columns. The difference in latencies of the responses evoked by stimulation of the dorsal column and the dorsolateral funiculus at the level of the insulating sheet is shown in the superimposed averaged responses in Fig. 1E. The latency difference is 1 msec which corresponds to the shortening of the latency obtained at increasing intensities of the stimulation of the dorsal column rostral or caudal to the insulating sheet. Responses obtained by peripheral stimulation of the contralateral foot pads on either side of the somatosensory cortex yielded positive-negative surface potentials with the same latency and amplitude indicating that no serious damage was caused to the spinal cord. The characteristics of the cortical responses obtained by electrical stimulation of the dorsal column and the lateral funiculus indicate that different pathways were activated. When the stimulus was applied at the level of an insulating sheet inserted lateral to the dorsal column, each of these pathways could be activated separately, independent of the stimulation intensity used. Stimulation at high intensity of the dorsal column or the lateral funiculus rostral or caudal to this sheet, however, elicited cortical potentials which had the characteristics of the response from both pathways, thus indicating a spread of current at the stimulation site. These results support previous studies which have indicated an efficient pathway in the dorsolateral funiculus separate from the dorsal column and with cortical projection. Our findings are in conflict with those of Whitehorn e t al. lo and Ennever and Towe a. Essentially the same technique with an electrical insulation between the dorsal column and the dorsolateral funiculus to prevent spread of current was used in our experiments and in those of Towe and co-workers. In our experiments, however, particular care was taken not to damage the fibres ascending in the dorsolateral funiculus, as well as to preserve the
362
Fig. 2. Specimenof histological section of the spinal cord at level C4-C5. Frozen section, 50/ma thickness. circulation in this region both during the dissection and during the insertion of the thin teflon sheet. Although some minor damage to the dorsal columns may have occurred it was in the present context most important not to interfere with the pathway in the dorsolateral funiculus. As shown by the histological specimen in Fig. 2 the longitudinal dissection left the dorsotateral funiculus intact. Although it is difficult to draw conclusions from the histological sections presented by Ennever and Towe, their lesions appear to a great extent to have involved the dorsal horn and may have interrupted ascending fibres as well as influenced the circulation to the nearby situated relay nucleus of the spinocervical tract, the lateral cervical nucleus. It should also be noted that in most of the previous studies indicating a short latency pathway projecting to the cortex via the dorsolateral funiculus, careful histological controls showed complete transverse lesions of the dorsal columnsl,~,5, 6,s,9 or complete bilateral hemisections of the spinal cord at C1 and C8, sparing only the fibres crossing the midline between the lesionsk Thus, it is concluded that the failure of Whitehorn e t al. ~° and Ennever and Towe 3 to observe responses in the somatosensory cortex, mediated via the lateral funiculus and with the previously described characters, is due to a damage to the appropriate pathway during the dissection or the insertion of the insulating mica plate between the dorsal column and the lateral funiculus. This work was supported by the Swedish Medical Research Council (Project No 14X-55).
363 1 ANDERSSON,S. A., Projection of different spinal pathways to the second somatic sensory area in cat, Acta physiol, scand., 56, Suppl. 194 (1962) 1-74. 2 CATALANO,J. V., ANDLAMARCHE,G., Central pathway for cutaneous impulses in the cat, Amer. J. Physiol., 189 (1957) 141-144. 3 ENNEVER,J. A., ANDTOWE, A. L., Response of somatosensory cerebral neurons to stimulation of dorsal and dorsolateral spinal funiculi, Exp. Neurol., 43 (1974) 124-142. 4 LEVITT, M., AND LEVITT,J., Sensory hind limb representation in the SmI cortex of the cat after spinal tractotomies, Exp. Neurol., 22 (1968) 276-302. 5 MARK, R. F., AND STEINER,J., Cortical projection of impulses in myelinated cutaneous afferent nerve fibres of the cat, J. Physiol. (Lond.), 142 (1958) 544-562. 6 MORIN,F., A new spinal pathway for cutaneous impulses, Amer. J. Physiol., 183 (1955) 245-252. 7 NORRSELL,U., AND VOORHOEVE,P., Tactile pathways from the hindlimb to the cerebral cortex in cat, Acta physiol, scand., 54 (1962)9-17. 8 NORRSELL,U., AND WOLPOW, E. R., An evoked potential study of different pathways from the hindlimb to the somatosensory areas in the cat, Acta physiol, scand., 66 (1966) 19-33. 90SCARSSON, O., AND ROS~N,I., Short-latency projections to the cat's cerebral cortex from skin and muscle afferents in the contralateral forelimb, J. Physiol. (Lond.), 182 (1966) 164-184. 10 WHITEHORN,D., MORSE,R. W., ANDTOWE,A. L., Role of the spinocervical tract in production of the primary cortical response evoked by forepaw stimulation, Exp. Neurol., 25 (1969) 349-364.
359
Does the spinocervical pathway exist?
S. A. A N D E R S S O N AND P. E. L E I S S N E R
Department of Physiology, University of Grteborg, Giiteborg 33 (Sweden)
(Accepted July 7th, 1975)
The existence of cortical responses of short latency to afferent volleys travelling in the dorsolateral funiculus of the spinal cord has been pointed out in many investigations1,2,5-9. Studies after selective lesions of the spinal cord at different levels have indicated that a synchronous volley ascending via the spinocervico-lemniscal pathway elicits a prominent positive-negative surface potential in the cortical areas SI and SII, with the same or shorter latency as that of an afferent volley mediated via the dorsal column. Single cortical units were also found to be excited with short latency from small contralateral receptive fields after lesions, leaving intact only the spinocervicolemniscal pathway1,4. Some authors3,10, using a method of direct electrical stimulation of the spinal cord, were not able to verify these effects. Instead, they found only a small positive or negative surface response in the somatosensory cortex after electrical stimulation of the dorsolateral funiculus at the cervical level of the spinal cord, when spread of current to the dorsal column was prevented by a mica plate inserted between the dorsal column and the lateral funiculus. After a lesion of the dorsal columns only few wide-field cortical neurones were influenced by peripheral adequate stimulation. These authors suggested that the short latency positive-negative potentials and the activation of cortical cells from small receptive fields, described by the previous investigators as due to activity in a pathway in the dorsolateral funiculus, in fact should be related to incomplete lesions of the dorsal columns and/or elimination of tonic interaction between two pathways. The present study was undertaken to elucidate this controversy by repeating the experiments of Towe and coworkers using a slight modification of their technique in order to minimize the damage to the dorsal horn and to fibres ascending in the dorsolateral funiculus. Two cats weighing 2.6 and 3.3 kg respectively were anaesthetized with 50 mg chloralose/kg i.p. and immobilized with decamethonium bromide i.v. Artificial respiration was given and the end-tidal pCOz was maintained at 4.5 ~. The body temperature was kept at 38 °C. Both cerebral hemispheres were exposed and the dorsal laminae of vertebrae Cz, C4 and C5 were removed. After opening the dura mater, the brain and the spinal cord were covered with warm mineral oil. An incision was made on one side in the pia mater along the dorsal root entry zone from mid C4 to mid C5. The dorsal column was then separated from the inner surface of the dorsal horn down
360 I
'U"
500 MA
I000 IAA
~
[ 1,300 pV rostr
~[
, .-.,_./ C
I [ I00 ~JV
I ~ X ~
5 mse¢ 25 msec
/
B
[ 400 pV
D 500 ~A J
HOOOpA
400 [JV
5 msec dorso~at funiculus stim.
Fig. 1. Arrangement of the stimulation electrodes and the appearance of the responses recorded from the somatosensory cortex at the indicated stimulation intensities applied to the contralateral cervical spinal cord. Stimulation at the dorsal column at the level of the insulating sheet (A) and at a more rostral location (B). Note the shorter latency in B. Stimulation of the dorsolateral funiculus at the level of the insulating sheet (C) and at a more rostral location (D). Note the notch in the initial positivity in D. E: Superimposed traces, showing the average responses of 16 consecutive stimulations of the dorsolateral funiculus and of the dorsal column respectively at the level of the insulating sheet and of the same stimulation intensity, 1000/~A. In all traces positivity is downwards. to the central canal leaving the blood vessels intact as much as possible. The dorsal column was tilted with the aid o f blunt glass hooks and a 0.2 m m × 15 m m x 15 mm teflon sheet was inserted under visual control between the dorsal column and the dorsolateral funiculus down to the central canal. Electrical stimulation could be delivered to pairs o f ball tipped A g - A g C I electrodes with an interelectrode distance o f 2.5 m m placed over the dorsal column and the dorsolateral funiculus, on either side as well as just rostral or caudal to the insulating teflon sheet (Fig. 1). Peripheral stimulation was carried out via pairs of needles, inserted in the central pads o f the fore- and hindpaws bilaterally. Stimulation was performed with 0.2 msec square pulses. The evoked cortical surface potentials were recorded via ball tipped A g - A g C I electrodes and fed into a conventional amplifying equipment with a low frequency cutoff(--3 dB) at l H z and a high frequency cutoff at 30 k H z and displayed on a CRO. Consecutive responses could be averaged on a Hewlett Packard, model 5480A. At the end o f the experiment the spinal cord was fixed in situ with 10 ~ formalin. The surgical interference with the dorsal column and the dorsolateral funiculus was examined microscopically in 50 # m frozen sections o f the spinal cord. Fig. 1 illustrates the arrangement o f the stimulating electrodes and the surface potentials evoked in the contralateral somatosensory area I. Electrical stimulation o f the dorsal columns caudal, medial or rostral to the insulating sheet (Fig. I A and B) elicited a positive-negative response in a large area o f the somatosensory cortex. The threshold response was obtained at an intensity o f about 50 #A. At stimulation intensities of more than two times the threshold, the characteristics and the distribution o f the cortical response remained virtually unchanged at different placements of the
361 stimulating electrodes on the contralateral dorsal co'.umn. The amplitude increased at higher stimulation intensities and could reach 1.5 mV at a stimulation strength of 0.5 mA. At low stimulation intensities the onset latency of the cortical response was about 5.5 msec, but the latency decreased to about 4.5 msec when a stimulation of high intensity, usually more than 5 times threshold, was applied to the dorsal columns rostral or caudal to the insulating sheet (Fig. 1B). No such shortening of the latency was found at stimulation of the dorsal columns at the level of the insulating sheet (Fig. 1A). Stimulation of the dorsolateral funiculus also elicited a positive-negative response at a similar intensity as stimulation of the dorsal column (Fig. 1C and D). The amplitude was about one third of that obtained with a corresponding stimulation intensity applied to the dorsal columns. The onset latency of the cortical response was about 4.5 msec and thus similar to the latency of the response elicited by high intensity stimulation of the dorsal column rostral to the insulating sheet. The characteristics and latencies of the cortical responses remained unchanged at increasing intensity of a stimulus applied to the lateral funiculus at the level of the insulating sheet. Stimulation of the dorsolateral funiculus with high intensities (1 mA) at sites caudal or rostral to the insulating sheet gave a notch (arrow) in the initial potential (Fig. 1D). Although the onset latency was the same as at lower stimulation intensities a second positivity appeared in the response at a latency similar to that of the positive potentials evoked via the dorsal columns. The difference in latencies of the responses evoked by stimulation of the dorsal column and the dorsolateral funiculus at the level of the insulating sheet is shown in the superimposed averaged responses in Fig. 1E. The latency difference is 1 msec which corresponds to the shortening of the latency obtained at increasing intensities of the stimulation of the dorsal column rostral or caudal to the insulating sheet. Responses obtained by peripheral stimulation of the contralateral foot pads on either side of the somatosensory cortex yielded positive-negative surface potentials with the same latency and amplitude indicating that no serious damage was caused to the spinal cord. The characteristics of the cortical responses obtained by electrical stimulation of the dorsal column and the lateral funiculus indicate that different pathways were activated. When the stimulus was applied at the level of an insulating sheet inserted lateral to the dorsal column, each of these pathways could be activated separately, independent of the stimulation intensity used. Stimulation at high intensity of the dorsal column or the lateral funiculus rostral or caudal to this sheet, however, elicited cortical potentials which had the characteristics of the response from both pathways, thus indicating a spread of current at the stimulation site. These results support previous studies which have indicated an efficient pathway in the dorsolateral funiculus separate from the dorsal column and with cortical projection. Our findings are in conflict with those of Whitehorn e t al. lo and Ennever and Towe a. Essentially the same technique with an electrical insulation between the dorsal column and the dorsolateral funiculus to prevent spread of current was used in our experiments and in those of Towe and co-workers. In our experiments, however, particular care was taken not to damage the fibres ascending in the dorsolateral funiculus, as well as to preserve the
362
Fig. 2. Specimenof histological section of the spinal cord at level C4-C5. Frozen section, 50/ma thickness. circulation in this region both during the dissection and during the insertion of the thin teflon sheet. Although some minor damage to the dorsal columns may have occurred it was in the present context most important not to interfere with the pathway in the dorsolateral funiculus. As shown by the histological specimen in Fig. 2 the longitudinal dissection left the dorsotateral funiculus intact. Although it is difficult to draw conclusions from the histological sections presented by Ennever and Towe, their lesions appear to a great extent to have involved the dorsal horn and may have interrupted ascending fibres as well as influenced the circulation to the nearby situated relay nucleus of the spinocervical tract, the lateral cervical nucleus. It should also be noted that in most of the previous studies indicating a short latency pathway projecting to the cortex via the dorsolateral funiculus, careful histological controls showed complete transverse lesions of the dorsal columnsl,~,5, 6,s,9 or complete bilateral hemisections of the spinal cord at C1 and C8, sparing only the fibres crossing the midline between the lesionsk Thus, it is concluded that the failure of Whitehorn e t al. ~° and Ennever and Towe 3 to observe responses in the somatosensory cortex, mediated via the lateral funiculus and with the previously described characters, is due to a damage to the appropriate pathway during the dissection or the insertion of the insulating mica plate between the dorsal column and the lateral funiculus. This work was supported by the Swedish Medical Research Council (Project No 14X-55).
363 1 ANDERSSON,S. A., Projection of different spinal pathways to the second somatic sensory area in cat, Acta physiol, scand., 56, Suppl. 194 (1962) 1-74. 2 CATALANO,J. V., ANDLAMARCHE,G., Central pathway for cutaneous impulses in the cat, Amer. J. Physiol., 189 (1957) 141-144. 3 ENNEVER,J. A., ANDTOWE, A. L., Response of somatosensory cerebral neurons to stimulation of dorsal and dorsolateral spinal funiculi, Exp. Neurol., 43 (1974) 124-142. 4 LEVITT, M., AND LEVITT,J., Sensory hind limb representation in the SmI cortex of the cat after spinal tractotomies, Exp. Neurol., 22 (1968) 276-302. 5 MARK, R. F., AND STEINER,J., Cortical projection of impulses in myelinated cutaneous afferent nerve fibres of the cat, J. Physiol. (Lond.), 142 (1958) 544-562. 6 MORIN,F., A new spinal pathway for cutaneous impulses, Amer. J. Physiol., 183 (1955) 245-252. 7 NORRSELL,U., AND VOORHOEVE,P., Tactile pathways from the hindlimb to the cerebral cortex in cat, Acta physiol, scand., 54 (1962)9-17. 8 NORRSELL,U., AND WOLPOW, E. R., An evoked potential study of different pathways from the hindlimb to the somatosensory areas in the cat, Acta physiol, scand., 66 (1966) 19-33. 90SCARSSON, O., AND ROS~N,I., Short-latency projections to the cat's cerebral cortex from skin and muscle afferents in the contralateral forelimb, J. Physiol. (Lond.), 182 (1966) 164-184. 10 WHITEHORN,D., MORSE,R. W., ANDTOWE,A. L., Role of the spinocervical tract in production of the primary cortical response evoked by forepaw stimulation, Exp. Neurol., 25 (1969) 349-364.
