Brain Research, 167 (1979) 385-390 ~) Elsevier/North-Holland Biomedical Press
385
Loci of joint cells in the cuneate and external cuneate nuclei of the cat
JULIAN MILLAR Department of Physiology, The London Hospital Medical College, London E1 2AD (U.K.)
(Accepted January l lth, 1979)
Although there has been considerable recent work on the physiology of primary joint afferents 3-5,7-11,1~,17, there is much less known about second-order cells in the joint afferent system. Many studies have shown that cells in the dorsal horn22, 23 and dorsal column nuclei (DCN) 2,6,12,19,20,24,25 respond specifically to joint movement, but if only movement stimuli are used, these studies cannot reliably discriminate cells driven by joint afferents from those driven by muscle afferents. Electrical stimulation of joint nerves is a reliable way to identify second-order cells, and has previously been used to locate joint cells in the dorsal horn13,14. Denervation of a limb except for joint afferents has been used to analyze gracile nuclei joint cells 1~, but this method does not allow convergence between modalities to be tested. Because recent work as suggested convergence between modalities in the joint cells of the cuneate nucleus, the present study used electrical stimulation of a joint nerve to map 'electro-anatomically' these joint cells. The elbow joint nerve (EJN) 1 was selected for stimulation. Cats weighing 2.5-3.5 kg were anaesthetized with pentobarbitone or a mixture of allobarbitone and urethane ('Dial'). With the head in a stereotaxic holder, the dorsal column nuclei were exposed and covered with warm mineral oil. The EJN was dissected out on one side and placed in a small silastic cuff containing fine silver-wire electrodes. A glass-coated tungsten microelectrode a6 was used to record extracellular spike activity from D C N neurons. There are very few cells in the DCN that can be driven from joint afferents. Hence a two-stage search strategy was used. Initially, the cuff electrodes were switched into a differential amplifier, and the tungsten microelectrode used to deliver 20-30/~A by 30 #sec square-wave current pulses at 20 Hz (tip, -ve). The electrode was then tracked across the DCN in a grid of penetrations spaced 100/~m apart on the surface of the nuclei. When the electrode came close to the joint afferent preterminal axons in the nuclei, antidromic action potentials could be recorded in the EJN (Fig. IA). From the loci of the lowest threshold points for antidromic excitation, the trajectory of the EJN afferents across the D C N was mapped. The cuff electrode was then switched into the stimulator and the tungsten electrode to the headstage, and using the same 20 Hz stimulation rate the nerve was stimulated with 20/zA by 30 #sec pulses.
386
A
D
E B
L
!
F C
L_.
Fig. 1. A: a pair of antidromic action potentials recorded in the elbow joint nerve from justthreshold stimulation in the cuneate nucleus. About 20 oscilloscope sweeps are superimposed during 20 Hz stimulation. The small antidromic spikes show no latency variability and overlap exactly, (A pair of antidromic spikes was often seen under these conditions. This may have been due to branching in the joint afferent fibre.) B: the electrodes in the same position as A but now recording in the nucleus and stimulating the joint nerve. A pair of spikes is produced from the cuneate cell at a latency slightly longer than the antidromic latency in A. The orthodromic volley in the preterminal afferent axon can just be seen at arrow. (Five sweeps superimposed during 20 Hz stimulation.) C - F : the same as in B b u t showing superimposed sweeps during half-second stimulation at 50 Hz, 100 Hz, 125 Hz and 200 Hz respectively. (The stimulus artefact appears twice in trace E and 3 times in F.) Horizontal scale: 1 msec for all traces. Vertical scale: B, 50 # V : C-F. 100 #V. Trace A no voltage calibration.
387 Cells responding to the stimulation were then sought along and below the trajectory of the afferents. (In several experiments cells were sought away from the afferents, but in no cases were cells found other than where antidromically mapped afferents were present.) Even with this technique the yield of cells was small, typically I 5 cells found per cat. When cells had been isolated they were marked by an electrolytic lesion (4-8 #A for 10 sec electrode tip, ÷ve). At the end of the experiment the brain was perfused in situ with 10 % formalin, fixed overnight and cut at 50 #m intervals in the plane of the electrode penetrations. Sections were stained with fast cresyl violet, and a projection microscope used to draw out the appearance of selected sections. A typical joint cell response is shown in Fig. 1. 1A shows antidromic responses in the EJN. I B shows the response with electrode positions unchanged, but the nerve stimulated and neuronal activity recorded through the tungsten microelectrode. A single cell is present, firing a pair of spikes per stimulus. The orthodromic activity of the preterminal joint afferents is just visible as a small notch on the trace (arrowed). 1C-F shows the cell responding at increasing frequencies of stimulation. The cell 'follows' the stimulus at up to 100 Hz (B D) but at greater frequencies (E and F) some stimuli fail to evoke a response. The latency to the n e x t stimulus in the train was reduced after a missed response as can be seen from the 'early' responses in E (arrowed). At high frequencies, many responses are missed and the latency becomes extremely erratic as in F. In all, 65 cells were recorded from and marked with lesions. Fig. 2 and 3 show the locations of these cells. Each cell is represented within the outline drawing of the transverse section in which the lesion appeared most clearly. (Lesions sometimes spanned two or 3 sections.) The outline of the lesion is shown in solid black. Only the part of the section containing the relevant cell masses is shown. The section drawings are arranged in order, so that the top left-hand outline in 2 is most rostral, moving down columns and then across rows for successively more caudal sections. The midline is shown on the right of each outline. The top left-hand outline in 3 is the next caudal section from the bottom righthand outline in 2. It can be seen that 15 cells were located in the external cuneate, and 50 cells in the cuneate. Only two cells were unequivocally sited in the rostral reticular zone of the cuneate (Fig. 2, column 2, sections 3 and 8), the rest lay in the cell cluster region. All cells responded with a burst of from 2 to 6 spikes to single shot stimuli to the nerve, with a latency between 3 and 8 msec. For any given cell, the latency did not vary by more than ~ 1 msec whether stimulated with a single shock or at 20 Hz. This suggests that they are monosynaptically connected to the joint afferents. It can be seen from Fig. 2 and 3 that the joint cells lie in a tube or column running rostrocaudally through the cuneate and external cuneate nuclei. In particular, it can be seen that only 5 or 6 cells were situated near the base of the cuneate nucleus. The remainder lay in a column running along the dorsolateral aspect of the cuneate and ventromedial aspect of the external cuneate nuclei. The base of the cuneate is where muscle afferents synapse ea, and where cells respond to movement of joints 19. The dorsal superficial cells in the cell cluster zone have cutaneous or hair receptive fields, and those in the region where the joint cells were located have receptive fields on
388 the antecubital aspect of the forelimb t9. In the present study, movement receptive fields could not be systematically studied due to the cuff electrodes on the joint nerve. However, of 47 cells tested, 25 main cuneate cells were found to have distinct superficial receptive fields in the skin around the cubital fossa. The cells responded with a burst of spikes to brushing the hairs within the field with a camel hair brush• (These cells are indicated in Fig. 2 and 3 by the letter H: in two cases a pair of cells was marked with a single lesion, these are indicated by H2). Using the limited amount of movement possible, it was found that a few cells(n = 6) without hair receptive fields did show slowly adapting responses to elbow extension, but the majority of cells were
z2
f ~
"
/2
t
Fig. 2.
\
389 e i t h e r u n r e s p o n s i v e o r g e n e r a t e d o n l y p h a s i c r e s p o n s e s to e l b o w m o v e m e n t s . N o e x t e r n a l c u n e a t e cells h a d h a i r r e c e p t i v e fields. T h u s , t h e r e is e v i d e n c e for c o n v e r g e n c e b e t w e e n c u t a n e o u s a n d j o i n t afferents on to cells in the c u n e a t e n u c l e u s . S i m i l a r c o n v e r g e n c e o f j o i n t , skin a n d t e n d o n o r g a n
N GNY
E:)
Figs. 2 and 3. Drawings of the sections containing lesions marking joint cells in the DCN. The area of the lesion is shown in solid black. Sections are arranged in rostrocaudal order, the most rostral in the top left-hand corner, most caudal in bottom right-hand corner. Fig. 3 is a continuation of Fig. 2. Sections from a number of different animals are shown, arranged relative to their distance rostral or caudal to obex. For compactness, only the parts of the sections containing the relevant nuclei are shown. Ceils with hair receptive field are marked H. Abbreviations: ECN, external cuneate nucleus; CN, main cuneate nucleus; GN, gracile nucleus.
390 a f f e r e n t s h a s b e e n i n t h e d o r s a l h o r n t4. T h i s s u g g e s t s t h a t s u c h c o n v e r g e n c e m a y b e a n i n t e g r a l p a r t o f t h e p r o c e s s i n g o f j o i n t a f f e r e n t i n f o r m a t i o n a t h i g h e r levels o f t h e nervous system. This work was supported by the Medical Research Council.
1 Andersen, H. T., K6rner, L., Landgren, S. and Silfvenius. H., Fibre components and cortical projections of the elbow-joint nerve in the cat. Acta physiol, scand.. 69 (1967) 373-382. 2 Brown, A. G., Gordon, G. and Kay, R. H., A study of single axons in the cat's medial lemniscus. J. Physiol. (Lond.J. 236 (1974) 225 246. 3 Burgess~P.R.andC~ark~F.J.~Characteristics~fkneeJ~intrecept~rsinthecat.J.Physhd.'Lm~d.j~ 203 (1969) 317-335. 4 Clark, F. J., Information signalled by sensory fibres in medial articular nerve. J. Neurophysiol.. 38 (1975) 1464-1472. 5 Clark, F. J. and Burgess, P. R., Slowly adapting receptors in cat knee joint: can they signal joint angle? J. NeurophysioL, 38 (1975) 1448-1463. 6 Gordon, G. and Paine, C. H.. Functional organisation of nucleus gracilis in cat, J. Physiol. Load.j, 153 (1960) 331 349. 7 Grigg, P., Mechanical factors influencing response of joint afferent neurons from cat knee, J. Neurophysiol., 38 ~1975) 1473 1488. 8 Grigg, P., Response of joint afferent neurons in cat medial articular nerve to active and passive movements of the knee. Brain Research. 118 (1976) 482-485. 9 Grigg, P. and Greenspan, B. J., Response of primate joint afferent neurons to mechanical stimulation of knee joint, J. NeurophysioL, 40 (1977) 1-8. 10 Heetderks, W. J.. Principal component analysis of neural population response of knee joint proprioceptors in cat, Brain Research, 156 (1978) 51-65. I I Horch. K. W.. Clark, F. J.. and Burgess, P. R.. Awareness of knee joint angle under static conditions. J. Neurophysiol., 38 (19751 1436 1447. 12 Kruger, L.. Siminoff, R. and Witkovsky, P.. Single neuron analysis of dorsal column nuclei and spinal nucleus of trigeminal in cat. J. Neurophysiot., 24 (1961) 333-349. 13 Lindstr6m, S. and Takata, M., Monosynaptic excitation of dorsal spinocerebellar tract neurons from low threshold joint afferents. Acta physiol, seand., 84 (1972) 430-432. 14 Lundberg, A., Malmgren, K. and Schomburg, E. D., Convergence from lb. cutaneous and joint afferents in reflex pathways to motoneurons, Brain Research, 87 (1975) 81-84. 15 McCall, W. D., Jr., Farias, M. C.. Williams. W. J. and Bement, S. L.. Static and dynamic responses of slowly adapting joint receptors. Brain Research, 70 (1974) 221-243. 16 Merrill, E. G. and Ainsworth. A., Glass-coated platinum-plated tungsten microeleetrodes, Med. Biol. Engng., 10 (1972) 662-672. 17 Millar, J., Flexion-extension sensitivity of elbow joint afferents in cat. Exp. Br~dn Res., 24 (1975) 209-214. 18 Millar, J.. Properties of identified joint cells in the cat. J. Physiol. (Lond.). 269 (1977) 36P. 19 Millar, J. and Basbaum, A. I.. Topography of the projection of the body surface of the cat to cuneate and gracile nuclei, Exp. Neurol., 49 (1975) 281-290. 20 Pert. 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. 21 Rosen. I.. Excitation of group 1 activated thalamocortical relay neurones in the cat. J. Physiol. (Lond.), 205 (1969) 237-255. 22 Wall, P. D., The laminar organisation of the dorsal horn and the effect of descending impulses. J. Physiol. (Lond.), 188 (1967) 403-423. 23 Wall, P. D., Dorsal horn electrophysiotogy. In A. lggo (Ed.), Handbook of Sensory Physiology. I1. Somatosensory System, Springer, Berlin, 1973. 24 Williams, W. J., Bement, S. L., Yin, T. C. T. and McCall, W. D. jr., Nucleus gracilis responses to knee joint motion : a frequency response study, Brain Research, 64 (1973) 123-140. 25 Winter, D. L., Nucleus gracilis of cat. Functional organisation and corticofugal effects, J. Neurophysiol., 28 (1965) 48-70.
385
Loci of joint cells in the cuneate and external cuneate nuclei of the cat
JULIAN MILLAR Department of Physiology, The London Hospital Medical College, London E1 2AD (U.K.)
(Accepted January l lth, 1979)
Although there has been considerable recent work on the physiology of primary joint afferents 3-5,7-11,1~,17, there is much less known about second-order cells in the joint afferent system. Many studies have shown that cells in the dorsal horn22, 23 and dorsal column nuclei (DCN) 2,6,12,19,20,24,25 respond specifically to joint movement, but if only movement stimuli are used, these studies cannot reliably discriminate cells driven by joint afferents from those driven by muscle afferents. Electrical stimulation of joint nerves is a reliable way to identify second-order cells, and has previously been used to locate joint cells in the dorsal horn13,14. Denervation of a limb except for joint afferents has been used to analyze gracile nuclei joint cells 1~, but this method does not allow convergence between modalities to be tested. Because recent work as suggested convergence between modalities in the joint cells of the cuneate nucleus, the present study used electrical stimulation of a joint nerve to map 'electro-anatomically' these joint cells. The elbow joint nerve (EJN) 1 was selected for stimulation. Cats weighing 2.5-3.5 kg were anaesthetized with pentobarbitone or a mixture of allobarbitone and urethane ('Dial'). With the head in a stereotaxic holder, the dorsal column nuclei were exposed and covered with warm mineral oil. The EJN was dissected out on one side and placed in a small silastic cuff containing fine silver-wire electrodes. A glass-coated tungsten microelectrode a6 was used to record extracellular spike activity from D C N neurons. There are very few cells in the DCN that can be driven from joint afferents. Hence a two-stage search strategy was used. Initially, the cuff electrodes were switched into a differential amplifier, and the tungsten microelectrode used to deliver 20-30/~A by 30 #sec square-wave current pulses at 20 Hz (tip, -ve). The electrode was then tracked across the DCN in a grid of penetrations spaced 100/~m apart on the surface of the nuclei. When the electrode came close to the joint afferent preterminal axons in the nuclei, antidromic action potentials could be recorded in the EJN (Fig. IA). From the loci of the lowest threshold points for antidromic excitation, the trajectory of the EJN afferents across the D C N was mapped. The cuff electrode was then switched into the stimulator and the tungsten electrode to the headstage, and using the same 20 Hz stimulation rate the nerve was stimulated with 20/zA by 30 #sec pulses.
386
A
D
E B
L
!
F C
L_.
Fig. 1. A: a pair of antidromic action potentials recorded in the elbow joint nerve from justthreshold stimulation in the cuneate nucleus. About 20 oscilloscope sweeps are superimposed during 20 Hz stimulation. The small antidromic spikes show no latency variability and overlap exactly, (A pair of antidromic spikes was often seen under these conditions. This may have been due to branching in the joint afferent fibre.) B: the electrodes in the same position as A but now recording in the nucleus and stimulating the joint nerve. A pair of spikes is produced from the cuneate cell at a latency slightly longer than the antidromic latency in A. The orthodromic volley in the preterminal afferent axon can just be seen at arrow. (Five sweeps superimposed during 20 Hz stimulation.) C - F : the same as in B b u t showing superimposed sweeps during half-second stimulation at 50 Hz, 100 Hz, 125 Hz and 200 Hz respectively. (The stimulus artefact appears twice in trace E and 3 times in F.) Horizontal scale: 1 msec for all traces. Vertical scale: B, 50 # V : C-F. 100 #V. Trace A no voltage calibration.
387 Cells responding to the stimulation were then sought along and below the trajectory of the afferents. (In several experiments cells were sought away from the afferents, but in no cases were cells found other than where antidromically mapped afferents were present.) Even with this technique the yield of cells was small, typically I 5 cells found per cat. When cells had been isolated they were marked by an electrolytic lesion (4-8 #A for 10 sec electrode tip, ÷ve). At the end of the experiment the brain was perfused in situ with 10 % formalin, fixed overnight and cut at 50 #m intervals in the plane of the electrode penetrations. Sections were stained with fast cresyl violet, and a projection microscope used to draw out the appearance of selected sections. A typical joint cell response is shown in Fig. 1. 1A shows antidromic responses in the EJN. I B shows the response with electrode positions unchanged, but the nerve stimulated and neuronal activity recorded through the tungsten microelectrode. A single cell is present, firing a pair of spikes per stimulus. The orthodromic activity of the preterminal joint afferents is just visible as a small notch on the trace (arrowed). 1C-F shows the cell responding at increasing frequencies of stimulation. The cell 'follows' the stimulus at up to 100 Hz (B D) but at greater frequencies (E and F) some stimuli fail to evoke a response. The latency to the n e x t stimulus in the train was reduced after a missed response as can be seen from the 'early' responses in E (arrowed). At high frequencies, many responses are missed and the latency becomes extremely erratic as in F. In all, 65 cells were recorded from and marked with lesions. Fig. 2 and 3 show the locations of these cells. Each cell is represented within the outline drawing of the transverse section in which the lesion appeared most clearly. (Lesions sometimes spanned two or 3 sections.) The outline of the lesion is shown in solid black. Only the part of the section containing the relevant cell masses is shown. The section drawings are arranged in order, so that the top left-hand outline in 2 is most rostral, moving down columns and then across rows for successively more caudal sections. The midline is shown on the right of each outline. The top left-hand outline in 3 is the next caudal section from the bottom righthand outline in 2. It can be seen that 15 cells were located in the external cuneate, and 50 cells in the cuneate. Only two cells were unequivocally sited in the rostral reticular zone of the cuneate (Fig. 2, column 2, sections 3 and 8), the rest lay in the cell cluster region. All cells responded with a burst of from 2 to 6 spikes to single shot stimuli to the nerve, with a latency between 3 and 8 msec. For any given cell, the latency did not vary by more than ~ 1 msec whether stimulated with a single shock or at 20 Hz. This suggests that they are monosynaptically connected to the joint afferents. It can be seen from Fig. 2 and 3 that the joint cells lie in a tube or column running rostrocaudally through the cuneate and external cuneate nuclei. In particular, it can be seen that only 5 or 6 cells were situated near the base of the cuneate nucleus. The remainder lay in a column running along the dorsolateral aspect of the cuneate and ventromedial aspect of the external cuneate nuclei. The base of the cuneate is where muscle afferents synapse ea, and where cells respond to movement of joints 19. The dorsal superficial cells in the cell cluster zone have cutaneous or hair receptive fields, and those in the region where the joint cells were located have receptive fields on
388 the antecubital aspect of the forelimb t9. In the present study, movement receptive fields could not be systematically studied due to the cuff electrodes on the joint nerve. However, of 47 cells tested, 25 main cuneate cells were found to have distinct superficial receptive fields in the skin around the cubital fossa. The cells responded with a burst of spikes to brushing the hairs within the field with a camel hair brush• (These cells are indicated in Fig. 2 and 3 by the letter H: in two cases a pair of cells was marked with a single lesion, these are indicated by H2). Using the limited amount of movement possible, it was found that a few cells(n = 6) without hair receptive fields did show slowly adapting responses to elbow extension, but the majority of cells were
z2
f ~
"
/2
t
Fig. 2.
\
389 e i t h e r u n r e s p o n s i v e o r g e n e r a t e d o n l y p h a s i c r e s p o n s e s to e l b o w m o v e m e n t s . N o e x t e r n a l c u n e a t e cells h a d h a i r r e c e p t i v e fields. T h u s , t h e r e is e v i d e n c e for c o n v e r g e n c e b e t w e e n c u t a n e o u s a n d j o i n t afferents on to cells in the c u n e a t e n u c l e u s . S i m i l a r c o n v e r g e n c e o f j o i n t , skin a n d t e n d o n o r g a n
N GNY
E:)
Figs. 2 and 3. Drawings of the sections containing lesions marking joint cells in the DCN. The area of the lesion is shown in solid black. Sections are arranged in rostrocaudal order, the most rostral in the top left-hand corner, most caudal in bottom right-hand corner. Fig. 3 is a continuation of Fig. 2. Sections from a number of different animals are shown, arranged relative to their distance rostral or caudal to obex. For compactness, only the parts of the sections containing the relevant nuclei are shown. Ceils with hair receptive field are marked H. Abbreviations: ECN, external cuneate nucleus; CN, main cuneate nucleus; GN, gracile nucleus.
390 a f f e r e n t s h a s b e e n i n t h e d o r s a l h o r n t4. T h i s s u g g e s t s t h a t s u c h c o n v e r g e n c e m a y b e a n i n t e g r a l p a r t o f t h e p r o c e s s i n g o f j o i n t a f f e r e n t i n f o r m a t i o n a t h i g h e r levels o f t h e nervous system. This work was supported by the Medical Research Council.
1 Andersen, H. T., K6rner, L., Landgren, S. and Silfvenius. H., Fibre components and cortical projections of the elbow-joint nerve in the cat. Acta physiol, scand.. 69 (1967) 373-382. 2 Brown, A. G., Gordon, G. and Kay, R. H., A study of single axons in the cat's medial lemniscus. J. Physiol. (Lond.J. 236 (1974) 225 246. 3 Burgess~P.R.andC~ark~F.J.~Characteristics~fkneeJ~intrecept~rsinthecat.J.Physhd.'Lm~d.j~ 203 (1969) 317-335. 4 Clark, F. J., Information signalled by sensory fibres in medial articular nerve. J. Neurophysiol.. 38 (1975) 1464-1472. 5 Clark, F. J. and Burgess, P. R., Slowly adapting receptors in cat knee joint: can they signal joint angle? J. NeurophysioL, 38 (1975) 1448-1463. 6 Gordon, G. and Paine, C. H.. Functional organisation of nucleus gracilis in cat, J. Physiol. Load.j, 153 (1960) 331 349. 7 Grigg, P., Mechanical factors influencing response of joint afferent neurons from cat knee, J. Neurophysiol., 38 ~1975) 1473 1488. 8 Grigg, P., Response of joint afferent neurons in cat medial articular nerve to active and passive movements of the knee. Brain Research. 118 (1976) 482-485. 9 Grigg, P. and Greenspan, B. J., Response of primate joint afferent neurons to mechanical stimulation of knee joint, J. NeurophysioL, 40 (1977) 1-8. 10 Heetderks, W. J.. Principal component analysis of neural population response of knee joint proprioceptors in cat, Brain Research, 156 (1978) 51-65. I I Horch. K. W.. Clark, F. J.. and Burgess, P. R.. Awareness of knee joint angle under static conditions. J. Neurophysiol., 38 (19751 1436 1447. 12 Kruger, L.. Siminoff, R. and Witkovsky, P.. Single neuron analysis of dorsal column nuclei and spinal nucleus of trigeminal in cat. J. Neurophysiot., 24 (1961) 333-349. 13 Lindstr6m, S. and Takata, M., Monosynaptic excitation of dorsal spinocerebellar tract neurons from low threshold joint afferents. Acta physiol, seand., 84 (1972) 430-432. 14 Lundberg, A., Malmgren, K. and Schomburg, E. D., Convergence from lb. cutaneous and joint afferents in reflex pathways to motoneurons, Brain Research, 87 (1975) 81-84. 15 McCall, W. D., Jr., Farias, M. C.. Williams. W. J. and Bement, S. L.. Static and dynamic responses of slowly adapting joint receptors. Brain Research, 70 (1974) 221-243. 16 Merrill, E. G. and Ainsworth. A., Glass-coated platinum-plated tungsten microeleetrodes, Med. Biol. Engng., 10 (1972) 662-672. 17 Millar, J., Flexion-extension sensitivity of elbow joint afferents in cat. Exp. Br~dn Res., 24 (1975) 209-214. 18 Millar, J.. Properties of identified joint cells in the cat. J. Physiol. (Lond.). 269 (1977) 36P. 19 Millar, J. and Basbaum, A. I.. Topography of the projection of the body surface of the cat to cuneate and gracile nuclei, Exp. Neurol., 49 (1975) 281-290. 20 Pert. 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. 21 Rosen. I.. Excitation of group 1 activated thalamocortical relay neurones in the cat. J. Physiol. (Lond.), 205 (1969) 237-255. 22 Wall, P. D., The laminar organisation of the dorsal horn and the effect of descending impulses. J. Physiol. (Lond.), 188 (1967) 403-423. 23 Wall, P. D., Dorsal horn electrophysiotogy. In A. lggo (Ed.), Handbook of Sensory Physiology. I1. Somatosensory System, Springer, Berlin, 1973. 24 Williams, W. J., Bement, S. L., Yin, T. C. T. and McCall, W. D. jr., Nucleus gracilis responses to knee joint motion : a frequency response study, Brain Research, 64 (1973) 123-140. 25 Winter, D. L., Nucleus gracilis of cat. Functional organisation and corticofugal effects, J. Neurophysiol., 28 (1965) 48-70.
