Three Ascending Tracts Activated from Group I Afferents in Forelimb Nerves of the Cat

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Three Ascending Tracts Activated from Group I Afferents in Forelimb Nerves of the Cat 0. O S C A R S S O N Institute of Physiology, University of Lund, Lund (Sweden)

The ascending projections of group I afferents from hindlimb muscles are well established. These afferents ascend in the dorsal funiculus for several segments but do not continue above the lower thoracic levels (Lloyd and McIntyre, 1950). The group I afferents make synaptic contacts with the cell bodies of the dorsal and ventral spino-cerebellar tracts (DSCT and VSCT) (Lloyd and McIntyre, 1950; Oscarsson, 1957a). The DSCT is uncrossed, ascends in the dorsal part of the lateral funiculus, and reaches the cerebAluni through the restiform body. It contains components activated monosynaptically from Ia and Ib muscle afferents (Lundberg and Oscarsson, 1956, 1960). The VSCT is crossed, ascends ventrally of the DSCT, and reaches the cerebellum through the brachium conjunctivuin. It receives monosynaptic excitation exclusively, or almost exclusively, from Ib afferents (Oscarsson, 1957b; Eccles et al., 1961a). There is no evidence that hindlimb group I afferents activate other ascending tracts or that collaterals of the DSCT and VSCT activate other structures than the cerebellum. Experiments made during the last two years have revealed that group I afferents in forelimb nerves activate three ascending tracts. One tract originates from cell bodies located at, or slightly above, the level of the dorsal root entrance, ascends in the middle third of the lateral funiculus, and terminates in the cerebellum. This tract i? anatomically and functionally distinct from the DSCT and VSCT and will be denoted the rostra1 spino-cerebellar tract (RSCT). The other two pathways are activated from group I afferents ascending in the dorsal funiculi to the cuneate nuclei (cf. Rexed and Strom, 1952). One of them originates from cells in the external cuneate nucleus and reaches the cerebellum through the ipsilateral restiform body as a component of the cuneo-cerebellar tract. The other pathway originates from the main cuneate nucleus and projects, via the crossed medial lemniscus, to the postcruciate gyrus of the cerebral cortex. THE ROSTRAL SPINO-CEREBELLAR TRACT

Ascending spinal tracts activated from forelimb nerves were recently investigated by recording from fascicles of the cord dissected at the third cervical segment. It was References p . 193-195

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shown that group I afferents in these nerves activate only one ascending tract. Some anatomical and functional characteristics of this tract were described and it was concluded that it is distinct from the spino-cerebellar tracts activated from hindlimb afferents (Holmqvist et al., 1963b). HINDLIMB IPSIL.

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Fig. 1. Discharges recorded at the third cervical segment from ascending spinal tracts on stimulation of ipsilateral and contralateral muscle nerves in the hindlimb (hamstring) and forelimb (deep radial). The stimulus strength was about 20 times the nerve threshold. The records were obtained from fascicles i-iii as indicated. The upper and lower traces show the discharges recorded simultaneously on a fast and slow time base. Middle traces in A-D show ascending volleys recorded from the dissected dorsal funiculi at C3. Time scales in msec. (Modified from Holmqvist and Oscarsson, 1963, and Holmqvist ef al., 1963b.)

The records in Fig. 1 show mass discharges in ascending tracts led from fascicles dissected as indicated on the diagram. Muscle nerves in the hind- and forelimbs were stimulated. The monosynaptic discharges evoked by impulses in group I afferents of hindlimb nerves are readily recognized. The DSCT discharge (A) is recorded from the ipsilateral, dorsal fascicle and the VSCT discharge (E) from the contralateral, intermediate fascicle. Only one tract is activated from group I afferents in forelimb nerves. This tract is ipsilateral and ascends in the intermediate fascicle. The discharge (H) is

Fig. 2. Relation between size of afferent volley and discharge evoked in the group 1 activated forelimb tract. Upper and lower traces show, at two speeds, the discharge evokcd by stimulation of the deep radial nerve at indicated strengths (multiples of nerve threshold). Middle traces show the ingoing volley recorded from the dissected dorsal funiculi at C3. From the experiment also illustrated in Fig. I . (Modified from Holmqvist et al., 1963b).

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comparable in size with the VSCT discharge and has a monosynaptic latency. The small early discharges recorded from the ipsilateral, dorsal fascicle (G) and from the contralateral, ventral fascicle (L) appeared only when the stimulus strength was raised to activate group I1 afferents. %

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Fig. 3. (A). Location of the group I activated forelimb tract at the level of the third cervical segment. The spinal cord sector containing this tract is indicated by vertical hatching. For comparison, the sectors are shown which contain the dorsal (horizontal hatching) and ventral (stippled) spino-cerebellar tracts. (B). Two experiments made to determine the segmental level of the cell bodies of the group I activated forelimb tract. In one experiment the dorsal funiculi were transected at successively more caudal levels (open circles), in the other the lateral funiculus was transected at successively more rostral levels (triangles), while the mass discharge was recorded from the dissected lateral funiculus at C3 on stimulation of the ipsilateral deep radial nerve. Ordinate: amplitude of monosynaptic discharge in per cent of control value. Abscissa: segmental level of transection after which the mass discharge was recorded and measured. The fourth cervical to second thoracic segments are indicated on the horizontal scale. See text. (Modified from Holmqvist et al., 1963b.)

The relation between the size of the ingoing volley and the mass discharge evoked in the forelimb tract is shown in Fig. 2. The discharge appeared at a strength of 1.3 (A, B), and grew to a maximum at 1.9 times threshold (D). I n other experiments the threshold varied between 1.2 and 1.4 and the maximum was reached at, or slightly below, maximum for the group I volley. The threshold for evoking the discharge is similar to the threshold of Ib (tendon organ) afferents in hindlimb nerves. The forelimb tract is presumably activated mainly or exclusively from Ib afferents, just as the VSCT. By recording from variously dissected fascicles it was shown that the group I activated forelimb tract ascends jn the middle third of the lateral funiculus at the C3 level. Its location relative to the DSCT and VSCT is shown in Fig. 3A. The forelimb tract (vertical hatching) is ventral of, but overlaps partly, the VSCT (stippled). The level of the synaptic relay in the cord was determined by transection of the dorsal funiculus (interruption of presynaptic fibres) at successively more caudal levels (circles) and by transection of the lateral funiculus (interruption of postsynaptic axons) at successively more rostral levels (triangles), while the reduction of the mass discharge was watched by recording from the lateral funiculus (Fig. 3B). The experiments show that the relay occurs at, or slightly above, the level of the dorsal root References p. 193-195

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entrance. These data show that the forelimb tract is anatomically distinct from DSCT and VSCT: it differs from DSCT in arising from cell bodies located rostrally of Clarke’s column and in having a ventral position in the cord, and from VSCT in being uncrossed. On the other hand, the group I activated forelimb tract resembles the VSCT in its termination and functional organization, as has been shown on recording from single units (Oscarsson and Uddenberg, unpublished). In the third cervical segment intraaxonal recording was made from fibres ascending in the lateral funiculus. Units that could be discharged from any of the dissected forelimb nerves were tested for antidromic activation from the cerebellar cortex, as had previously been done with units in the DSCT and VSCT (Lundberg and Oscarsson, 1960, 1962). The great majority of the units that were monosynaptically activated from group I afferents in ipsilateral forelimb nerves could be antidromically activated from the cerebellum. The group I activated tract was denoted the rostral spino-cerebellar tract (RSCT) as it terminates in the cerebellum and originates from cell bodies in the rostral part of the cord. A typical RSCT unit is shown in Fig. 4. In records A-F and I the deep radial (DR) nerve was stimulated at increasing strengths. A spike appeared irregularly at 1.3 A

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Fig. 4. Recording from RSCT axon (lower traces) and recording from the surface of the dorsal funiculi in C3 (upper traces). The stimulating and recording arrangements are shown in diagram P. The following nerves were stimulated: ipsilateral deep radial nerve (DR), ipsilateral nerve to long head of triceps (LHT), ipsilateral nerve to biceps (B), ipsilateral median nerve (M), ipsilateral superficial radial nerve (SR), and contralateral radial nerve (r. R). A-F were obtained at the stimulus strengths indicated in multiples of the nerve threshold and G-L at about 15 times threshold. M and N show antidromic spikes elicited from the cerebellar cortex on stimulation of the points indicated in the diapram of the explored part of the anterior cerebellar lobe (0)(cf. Fig. 6). Larsell’s lobules IV and V are indicated. The interrupted line separates hind- and forelimb areas. Records M and N were obtained at faster speed than A-L. (From unpublished observations of Oscarsson and Udden berg.)

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times threshold when the ingoing volley (upper traces) was about one third maximal. The spike came regularly at higher strengths and a second spike was evoked by impulses in group I1 afferents when the strength was raised to 2.7 times threshold. Further increase of stimulus strength produced further spikes. Stimulation of the ipsilateral biceps nerve (B) was ineffective as was stimulation of the contralateral radial nerve (r. R). However, late spikes appeared with stimulation of low threshold afferents in the superficial radial nerve (SR) and of high threshold afferents in the nerve to the long head of triceps (LHT) and the median nerve (M). Records M and N show antidromic spikes evoked by weak electrical stimulation of the points indicated in the diagram of the anterior lobe (0). Similar observations were made with the other group I activated units. A monosynaptically evoked spike appeared on stimulation of high threshold group I afferents in one or more nerves. In similarity with the VSCT there was very often convergence of group I excitation from muscle groups working at d.ifferent joints: one group of RSCT units was activated both from extensors of the hand and extensors of the forearm and another group from flexors of the hand as well as extensors of the forearm. As in VSCT, no convergence was observed from antagonists working at the same joint (Eccles et al., 1961a). Presumably the RSCT units forward information concerning stages of movement or position of the whole limb rather than information of increased tension in individual muscles, just as has been suggested for the VSCT (Oscarsson, 1960). The group I activated units usually received polysynaptic excitation from the flexor reflex afferents in one or several ipsilateral nerves. Inhibitory action from the flexor reflex afferents was sometimes noted. Though the RSCT units are polysynaptically influenced from the flexor reflex afferents in similarity with the VSCT units (Oscarsson, 1957b; Eccles et al., I961a), they differ from the latter in that the synaptic actions of these afferents are not predominantly inhibitory as in VSCT. This is also

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Fig. 5 . Effect produced by a conditioning cutaneous voiley on mass discharges in DSCT, VSCT and RSCT. The tract discharges were recorded from the dissected lateral funiculus at the C3 level on stimulation of group I afferents in the ipsilateral (DSCT) and contralateral (VSCT) hamstring nerve and on combined stimulation of group I afferents in the deep radial nerve and the nerve to the long head of triceps (RSCT). The conditioning volleys were obtained by stimulation of the ipsilateral sural (DSCT), controlateral sural (VSCT), and ipsilateral superficial radial (RSCT) nerve at a strength of about 10 times threshold. Abscissa: volley interval in msec. Ordinate: amplitude of conditioned discharge in per cent of control value. 0-0 = RSCT; A-A = VSCT; X - x = DSCT. (From unpublished observations of Oscarsson and Uddenberg.) References p . 193-195

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demonstrated in Fig. 5. In the same preparation the monosynaptic discharges in DSCT, VSCT and RSCT were conditioned by a preceding volley in cutaneous afferents from the same limb that supplied the monosynaptic excitation. The VSCT was strongly and the DSCT weakly inhibited (Oscarsson, 1957b), whereas the RSCT was facilitated. In other experiments the RSCT mass discharge was either facilitated or weakly inhibited by conditioning volleys in the flexor reflex afferents. The termination areas of the three spino-cerebellar tracts are shown in Fig. 6. Only DSCT

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Fig. 6 . Cerebellar termination of left DSCT, VSCT, and RSCT. The diagram refers to the culmen of the anterior cerebellar lobe with Larsell’s lobules IV and V indicated. The curved line represents the rostra1 border of the exposed part of the anterior lobe. The interrupted line separates hindlimb and forelimb areas. Vertical lines indicate borders of intermediate cortices, horizontal lines sulci. (Data compiled from Lundberg and Oscarsson, 1960, 1962, and from unpublished observations of Oscarsson and Uddenberg.)

the culmen of the anterior lobe was explored in detail. Larsell’s lobules IV and V are indicated and the interrupted line shows the boundary between the hind- and forelimb areas according to anatomical (Grant, 1962b) and physiological investigations (Grundfest and Campbell, 1942; Snider and Stowell, 1944; Carrea and Grundfest, 1954; Combs, 1954). The dots indicate points from which individual units could be activated antidromically at a low stimulus strength. The DSCT terminates almost exclusively in the ipsilateral intermediate cortex, whereas the VSCT and RSCT terminate bilaterally in longitudinal zones consisting of a medial strip of the intermediate cortex and a lateral strip of the vermal cortex. Another similarity of the VSCT and RSCT units is that many of them can be activated antidromically from more than one point, often one ipsilateral and one contralateral, indicating branching of single fibres. Contralateral termination is most common with the VSCT units, whereas ipsilateral termination occurs more often with the RSCT units. This might be connected with the contralateral location of the VSCT cells and the ipsilateral location of the RSCT cells. The DSCT and VSCT terminate almost exclusively in the hindlimb area, whereas the RSCT units terminate approximately equally often in the hindlimb area as in the forelimb area. The bilateral termination areas of the VSCT and RSCT might indicate that the information conveyed by these tracts is used in the motor coordination of ipdateral

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and contralateral limbs. The termination of the RSCT in both hindlimb and forelimb areas might correspondingly indicate that the information is used for the coordination of fore- and hindlimb movements. This tallies well with the hypothesis that the information mediated by these tracts concerns stages of movement or position of the whole limb. On the other hand, the DSCT units have small receptive fields and terminate ipsilaterally. It is possible that the information conveyed by these units is used mainly for the adjustment and coordination of movements within the ipsilateral limb. In this context it is interesting that the DSCT seems to terminate in the intermediate cortex, whereas the VSCT and RSCT have a more medial termination including a lateral strip of the vermis. According to Chambers and Sprague (1955a, b) each intermediate cortex regulates ‘the spatially organized and skilled movements and the tone and posture associated with these movements of the ipsilateral limbs’ and each vermal cortex, ‘tone, posture, locomotion, and equilibrium of the entire body’ (cf. also Pompeiano, 1958). THE CUNEO-CEREBELLAR TRACT

The cuneo-cerebellar tract originates from cells in the external cuneate nucleus and reaches cerebellum through the ipsilateral restiform body (Ferraro and Barrera, 1935). The external nucleus receives afferents from the dorsal funiculus but from no other known sources. The cuneo-cerebellar tract has, mainly on anatomical grounds, been assumed to be a forelimb homologue of the DSCT (Blumenau, 1891 ; Sherrington, 1890, 1893; Ferraro and Barrera, 1935; Brodal, 1941 ; Grant, 1962a). This hypothesis has now been substantiated by results obtained in an electrophysiological investigation of the tract (Holmqvist et al., 1963a). The mass discharge in the cuneo-cerebellar tract was recorded monophasically from the ‘dissected restiform body’ prepared as described by Holmqvist et al. (1963a). The spinal cord was almost completely transected sparing only the dorsal funiculi so as to exclude interference by activity in other ascending tracts. Records A-F in Fig. 7 show the mass discharge evoked by stimulation of the ipsilateral deep radial nerve at the indicated strengths. The first spike-like discharge appeared before any ingoing volley was discernible (A), showing that transmission through the external cuneate nucleus occurs with very little need for spatial summation. The first two spikes of the mass discharge were entirely due to excitation produced by the group I volley (A-D) ; the third spike was partly due to group I and partly to group I1 activation. At higher strengths of stimulation a late, prolonged discharge was added (E, F). Records G-L show the discharge evoked by stimulation of cutaneous afferents in the superficial radial nerve. Contralateral nerves were always ineffective (M, N). The units contributing to the mass discharge in the cuneo-cerebellar tract were analysed by intra-axonal recording from fibres in the region indicated by the dotted line in the diagram of Fig. 7. The results show that the tract contains one proprioceptive and one exteroceptive subdivision. The former consists of units activated monosynaptically from group I muscle afferents. One unit activated from the deep radial nerve is shown in Fig. 8. One or two impulses were discharged at a strength References p . 193-195

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Fig. 7. Mass discharges recorded from the dissected restiform body on stimulation of ipsilateral and contralateral muscle (deep radial) and skin (superficial radial) nerves in the forelimbs (IM, CM, IS, CS). The spinal cord was transected at C3 except for the dorsal funiculi. Upper two traces in each set of records show, on a fast time base, the ingoing volley recorded triphasically from the dorsal funiculi at C3 and the mass discharge in the restiform body. Lower trace shows the mass discharge on a slow time base. Stimulus strengths, in multiples of threshold for evoking a mass discharge, are indicated in A-L. The stimulus strength in M and N was at 20 times threshold. Dots mark stimulus artefacts. Voltage scale refers to mass discharge recording. The diagram describes the recording conditions. The ‘dissected restiform body’ was prepared as follows. The cerebellum was sucked away leaving the peduncles and adjacent white matter intact. The brachium conjunctivum and brachium rontis were cut through along the interrupted line. A loop tied to the peduncles was hooked into one c f the recording electrodes and used for lifting the ‘dissected restiform body’ from underlying tissue (not shown). The other recording electrode was placed against the ‘dissected restiform body’ where it was in continuity with the brain stem at the rostra1 border of the eighth nerve. Axonal recording was performed within the area surrounded by the dotted line. (Modified from Holmqvist et al., 1963a.)

evoking no perceptible ingoing volley (A) and four or five spikes appeared at a strength of about 1.2 times threshold (C). No additional impulses were elicited when the stimulus was increased to supramaximal for group I afferents (F). Stimulation of the ipsilateral skin nerve (G) and contralateral nerves (H, I) evoked no activity. The other units activated from group I afferents were similar. Ths first impulse appeared at a very low stimulus strength and a large group I volley almost always produced a repetitive response. There was never additional activation from group I I and I11 muscle afferents or from skin afferents. The response to stretch of musclc was a slowly adapting discharge and the receptive field was one or a few adjaccnt muscles. The group I activated units in the DSCT have similar characteristics (Laporte et al., 1956; Lundberg and Oscarsson, 1956; Holmqvist et al., 1956; Lundberg and Winsbury, 1960; Eccles et al., 1961b). They are monosynaptically activated from group I muscle

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afferents in one or a few muscle nerves and the response is often repetitive. The DSCT units do not reczive additional excitation from group IT1 muscle afferents and cutaneous afferents but they are, presumably in contrast with the cuneo-cerebdlar units, sometimes activated from group TI muscle afferents. The DSCT contains one functional subgroup activated from Ia and another from Ib afferents. It is unknown if there are two corresponding subgroups in the cuneo-cerebellar tract. The exteroceptive subdivison in the cuneo-cerebellar tract will not be described in detail. It consists of units activated from cutaneous afferents and often also from high threshold (group TI and 111) muscle afferents. There are several subgroups which

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Fig. 8. Cuneo-cerebellar unit activated from group I muscle afferents. Upper two traces in each set of records show, on a fast time base, microelectrode recording from the axon and recording from surface of the dorsal funiculi at C3; lower two traces show, on a slow time base, microelectrode recording from the axon and recording from dissected restiform body. A-F were obtained on stimulation of the ipsilateral muscle (deep radial) nerve (IM) at indicated strengths in multiples of mass discharge threshold. G I show that no discharge was elicited by stimulation (at 20 times threshold) of the ipsilateral skin (superficial radial) nerve (IS) or of the contralateral muscle and skin nerves (CM, CS). Superposed sweeps. Time scales in msec. (From Holmqvist et al., 1963a.)

correspond largely to those described previously for the exteroceptive subdivision in the DSCT (Lundberg and Oscarsson, 1960). However, the exteroceptive units in the cuneo-cerebellar tract differ, in one respect, conspicuously from those in the DSCT. The DSCT units are monosynaptically activated from cutaneous afferents, whereas the corresponding cuneo-cerebellar units are disynaptically activated from these afferents as well as from the sometimes converging high threshold muscle afferents. CEREBRAL PROJECTION OF GROUP 1 AFFERENTS

It is generally conccded that group I afferents from stretch receptors in hindlimb muscles do not project to the cerebral cortex (Mountcastle et al., 1952; McIntyre, 1962). However, a cerebral projection of forelimb group I afferents was suggested by References p. 193-195

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th: findings of Amassian and Berlin (1958). These observations have now been confirmed and extended (Oscarsson and Roskn, 1963a, b).

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Fig. 9. Evoked potentials recorded from the somatic area I (SI) and 11 (SII) on stimulation of the contralateral deep radial nerve. The potentials were simultaneously recorded on a fast (left traces) and slow time base. The inset records (upper left traces) show, on the fast time base, the primary afferent volley triphasically recorded from the dorsal funiculus at the C3 level immediately after the cortical recording. Stimulus strength in multiples of nerve threshold is indicated on each set of records. Positivity is signalled upwards. Voltage scale applies to cortical potentials (right traces). (From Oscarsson and RosCn, 1963a.)

Records A-E in Fig. 9 show surface-positive potentials evoked in the first somatic area (SI) on stimulation of group 1 muscle afferents in the contralateral deep radial nerve. The cortical potentials appeared at a strength producing a hardly visible ingoing volley (upper traces, A) and grew to a maximum with the group I volley (B-D). Additional activation of high threshold afferents did not increase the amplitude further but caused some increase of the following negative potential (E). On the other hand, in the second somatic area potentials appeared only when the strength was increased to activate group 11 afferents (F-J). Similar observations were made on stimulation of nerves to single muscles, for example the nerves to extensor carpi radialis, extensor digitorum communis, biceps, and the long head of triceps. The potentials evoked from group 1 afferents were limited to a small part of the forelimb region of SI, as defined by Woolsey and collaborators (Woolsey, 1947, 1959) (Fig. 10A). The group I potentials occurred only in the rostra1 part of this region, in the area between the postcruciate dimple and the cruciate sulcus. The responsive area was denoted R-SI and is shown schematically in Fig. 1OC. On the other hand, the potentials evoked from cutaneous and high threshold muscle afferents had two maxima, one in R-SI and the other in an area caudally of the dimple denoted C-SI (Fig. 1OC). These observations indicate that the forelimb region of S1 is differentiated

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Fig. 10. Dorsal view of the rostra1 pole of the cerebral hemisphere to show the forelimb region of the first somatic area (SI). The ansate, coronal, and cruciate sulci and the postcruciate dimple are indicated in A. (A). The area enclosed by the interrupted line shows the forelimb region of SI according to Woolsey (1947, 1959). (B). The area enclosed by the interrupted line shows the cortex responding to tactile stimulation of the forelimb and the hatched area, the cortex from which forelimb motor responses could be elicited in the experiments of Livingston and Phillips (1957). (C). Location of the responsive areas, C-SI and R-SI, discussed in the present paper. (From Oscarsson and Rosen, 1963b.)

into two parts with different function. It is tempting to associate R-SI with the motor and C-SI with the sensory cortex. Livingston and Phillips (1957) mapped, in the same experiments, the cortical areas responsive to tactile stimulation and those from which movements could be elicited. The forelimb regions of these areas are shown in Fig. 10B: the interrupted line encloses the responsive area and the hatched field shows the ‘motor’ area. The latter corresponds remarkably well to R-SI of the present investigation, though it extends more rostrally. Presumably the group 1 projection to the cerebral cortex represents a feedback channel used for adjusting the motor output from the cortex. The receptors of the group I afferents projecting to the cerebral cortex were identified by natural stimulation. A discharge from the appropriate receptors could be recognized by the depression of the cortical potential evoked on electrical stimulation

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Fig. 11. Change in amplitude of cortical potential evoked by a volley in Group I afferents of the nerve to extensor digitorum communis (EDC), on loading the tendon with various weights (A) and after close arterial injection of succinylcholine chloride (B). Ordinate: amplitude of the surface-positive cortical potential in per cent of control value obtained before loading (A) and injection (B). Abscissa: time in seconds after beginning of loading (A); time in minutes after injection (B). Interrupted vertical line in A indicates release from loading. Filled circles in B show absence of effect after transection of the EDC nerve. (From Oscarsson and Rosen, 1963b.) References p. 193-195

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of the intact nerve. This depression may be correlated with the marked reduction of the cortical potential that occurs at even low repetition rates of stimulation in the anaesthetized preparation. Fig. 11A shows the reduction of the potential evoked by stimulation of the nerve to extensor digitorum communis, on loading the muscle tendon with 10, 20 and 100 g. 10 g was sufficient to cause a definite depression and larger loads produced a marked reduction of the cortical potential. There was an initial phase of strong depression followed by a moderate one that remained until the end of the loading. Presumably the time course of the depression reflects the

Fig. 12. Relation between size of afferent volley and discharge evoked in medial IemnisLus and cuneo-cerebellar tract. The deep radial nerve was stimulated a t indicated strengths (multiples of nerve threshold). The traces show from above downwards: the lemniscal discharge and the ingoing volley at a fast speed, and the lemniscal discharge and the discharge in the cuneo-cerebellar tract at a slow speed. Positivity is signalled upwards. The lemniscal discharge was recorded with a steel needle electrode in the region of the lemniscus at a low pons level. The discharge in the cuneo-cerebellar tract was recorded from the dissected restiform body as described in Fig. 7. The ingoing volley was recorded triphasically from the dorsal funiculi at C3. Time scales in msec. (Partly unpublished records by Oscarsson and Rosen.)

adaptation of the receptors. Fig. 1 IB shows the depression of the cortical potential that occurred after close arterial injection of succinylcholine which is known to evoke a discharge in muscle spindle, but not in tendon organ afferents (Granit et a/., 1953). Following transection of the nerve the effect was abolished (filled circles). It was concluded from these and other experiments that group I afferents projecting to the cerebral cortex originate from muscle spindles, but an additional projection from tendon organs can not be excluded. The group I projection path belongs to the dorsal funiculus-medial lemniscus system. The cortical potentials evoked from group I afferents disappeared after a lesion in the dorsal funiculi but remained after almost complete transection of the cord sparing these funiculi. Additional confirmation was obtained on recording from the medial lemniscus at the pons level: the expected discharge appeared on stimulation of group I afferents in contralateral forelimb nerves (Fig. 12). The findings described in this and the previous section indicate that group 1 afferents ascending in the dorsal funiculi activate neurones in the external as well as in the main cuneate nucleus. The neurones of the external nucleus give origin to the uncrossed cuneo-cerebellar tract and the neurones of the main nucleus to the crossed medial lemniscus. The properties of the group I relays in the two nuclei were compared by simultaneous recording from the two tracts on stimulation of the deep radial nerve. The traces in Fig. 12 show from above downwards: the lemniscal discharge and the ingoing volley at a fast speed, and the lemniscal discharge and the discharge

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in the cuneo-cerebellar tract at a slow speed. A discharge with a monosynaptic latency appeared in both tracts at a very low stimulus strength producing a hardly visible ingoing volley (A). The initial part of the discharge grew to a maximum with the group I volley (B-D) and additional activation of high threshold afferents prolonged the activity. An input-output curve obtained from a similar experiment is shown in Fig. 13A. Triangles represent the amplitude of the lemniscal discharge

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Fig. 13. (A). Input-output curve for transmission of impulses from group I afferents through the main and external cuneate nuclei. The deep radial nerve was stimulated. Abscissa: amplitude of ingoing volley recorded triphasically from the dorsal funiculus at C3. Ordinate: amplitude of mass discharge in medial lernniscus (triangles) and cuneo-cerebellar tract (crosses). (B). Effect of frequency on transmission through the main and external cuneate nuclei. The deep radial nerve was stimulated. Abscissa: stimulation frequency (log scale). Ordinate : amplitude of mass discharge in medial lemniscus (triangles) and cuneo-cerebellar tract (crosses) in per cent of value at a frequency of l/sec. Each point was obtained from superposed records when a steady state was attained, e.g. after 10-20 stimuli at the high frequencies. (Modified from Oscarsson and Rosen, 1963b.)

and crosses, the amplitude of the discharge in the cuneo-cerebellar tract. The curve fits both sets of points suggesting that, at both relays, the same types of afferents were responsible for the postsynaptic discharge and that transmission through both nuclei occurs with little need for spatial summation. On the other hand, the two group I relays differ in their ability to transmit impulses at high frequencies. The mass discharge in the lemniscus decreased at frequencies above 10, and that in the cuneo-cerebellar tract only at frequencies above 75/sec (Fig. 13B). In its ability to follow high frequencies the group I relay in the external cuneate nucleus is similar to the group I relays of the DSCT and VSCT (Holmqvist et al., 1956; Oscarsson, 1957b), whereas the relay in the main nucleus is intermediate between these relays and the monosynaptic connections between group I afferents and motoneurones (Adrian and Bronk, 1929; Lloyd and Wilson, 1957). It seems likely that the ability to follow high frequencies is related to the properties of the next synaptic relays. There is evidence suggesting that the thalamic relay has a pronounced recurrent inhibition (Andersen and Eccles, 1962) which presumably limits the transmission at high frequencies, whereas at least some neurones in the cerebellar cortex may follow very high frequencies of orthodromic stimulation (Granit and Phillips, 1956). COMMENTS

Group I afferents in hindlimb nerves have two ascending projections, the dorsal and the ventral spino-cerebellar tract. It must now be recognized that group J afferents in References p . 193-195

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forelimb nerves have three projections, two terminating in the cerebellar cortex and one in the cerebral cortex. It is of interest to compare the hind- and forelimb projections and to discuss possible reasons for differences between them. The cuneo-cerebellar tract is obviously a forelimb homologue of the DSCT. The two tracts are largely equivalent as channels for proprioceptive and exteroceptive information. Ln both tracts the proprioceptive subdivision consists of units monosynaptically activated from group I muscle afferents and carrying information with a high degree of spatial discrimination. The exteroceptive subdivision has a similar functional organization in the two tracts but is monosynaptically activated from cutaneous afferents in the DSCT and disynaptically, in the cuneo-cerebellar tract. The reason for this discrepancy is unknown but might be connected with an earlier synaptic relay in the main cuneate nucleus (Holmqvist et al., 1963b). The rostral spino-cerebellar tract is anatomically distinct from the DSCT and VSCT but resembles functionally the latter tract. It can be regarded as a functional forelimb equivalent of the VSCT. RSCT units are monosynaptically activated from lugh threshold group I afferents, presumably identical with tendon organ (Ib) afferents. There is very often convergence of group I excitation from muscles working at different joints suggesting that the RSCT conveys information about stages of movement or position of the whole limb, as has previously been suggested for the VSCT (Oscarsson, 1960). The RSCT differs from the VSCT in that the polysynaptic effects from the flexor reflex afferents are not predominantly inhibitory as in the latter tract. The functional significance of this difference is obscure. Another difference relates to the termination of the two tracts. The VSCT terminates almost exclusively in the hindlimb area of the cerebellar cortex, whereas the RSCT terminates in the forelimb as well as the hindlimb area. Possibly the information carried by RSCT is more directly utilized in the coordination of fore- and hindlimb movements. The projection of group I afferents to the cerebral cortex through the dorsal funiculus-medial lemniscus system has no hindlimb equivalent. The forelimbs are used not only in locomotion but also in a wide variety of other movements, such as handling and perhaps exploration of the environment. This might necessitate a direct feedback channel for the control of movements elicited from the cortex, whereas hindlimb movements might be controlled mainly through reflex mechanisms at lower levels. The group I projection presumably represents such a feedback system and it is significant that it terminates in a rostral part of the postcruciate gyrus which probably is a motor area in the cat. Our findings demonstrate marked differences between ascending pathways related to the h n d - and forelimb levels respectively. Group I afferents project to the cerebellar cortex through two ‘forelimb’ and two functionally equivalent ‘hindlimb tracts’. The functional organization of each forelimb tract is similar to, but not identical with, the functional organization of the corresponding hindlimb tract and the anatomical organization is different. The cerebral projection of Group I afferents is related exclusively to the forelimb level. Obviously, these results call for considerable caution when transferring observations on tracts originating from one segmental level of the body to those originating from another level.

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SUMMARY

Group I muscle afferents in hindlimb nerves activate two ascending tracts, the dorsal and the ventral spino-cerebellar tract (DSCT and VSCT). Recent investigations show that group I afferents in forelimb nerves activate three ascending pathways. 1. The rostra1 spino-cerebellar tract (RSCT) originates from cell bodies at, or slightly above, the level of the dorsal root entrance, ascends ipsilaterally in the middle third of the lateral funiculus, and terminates in a characteristic manner in the anterior cerebellar lobe. It receives monosynaptic excitation from high threshold group I muscle afferents, presumably identical with tendon organ afferents. Convergence of group 1 excitation from muscles working at different joints is common suggesting that the RSCT forwards information concerning stages of movement or position of the whole limb rather than information about increased tension in individual muscles. It is suggested that the RSCT is a functional forelimb homologue of the VSCT. 2. The cuneo-cerebellar tract contains one component that is monosynaptically activated from very low threshold group I muscle afferents, presumably identical with muscle spindle afferents. The response to a single volley in group I afferents is repetitive and transmission can occur at very high frequencies. The receptive field is small; it often consists of a single muscle. Other components of the cuneo-cerebellar tract are disynaptically activated from cutaneous afferents. It is concluded that the cuneocerebellar tract is a forelimb equivalent to the DSCT. 3. The third pathway is a projection to the cerebral cortex of large muscle spindle afferents. The group I afferents ascend in the dorsal funiculus and activate monosynaptically cells in the main cuneate nucleus which give origin to a component of the medial lemniscus. After a presumed thalamic relay the projection terminates in a small cortical area between the cruciate sulcus and the postcruciate dimple. It is suggested that this area has a motor function in the cat. The group I projection is presumably a feedback system used for the control of movements elicited from the cortex. The cerebral projection of forelimb group I afferents has no hindlimb equivalent. REFERENCES ADRIAN, E. D., A N D BRONK,D. W., (1929); The discharge of impulses in motor nerve fibres. Part 11. The frequeniy of discharge in reflex and voluntary contractions. J. Physiol. (Lond.), 67, 119-151. AMANAN,V. E., AND BERLIN,L., (1958); Early cortical projection of Group I afferents in the forelimb muscle nerves of cat. J . Physiol. (Lond.), 148, 61P. ANDERSEN, P., AND ECCLES,J. C., (1962); Inhibitory phasing of neuronal discharge. Nature (Lond.), 196, 645-647. L., (1891); Ueber den ausseren Kern des Keilstranges im verlangerten Mark. Neurol. BLUMENAU, Cbl., 10, 226-232. BRODAL, A., (1 941); Die Verbindungen des Nucleus cuneatus externus mit dem Kleinhirn beim Kaninchen und bei der Katze. Experimentelle Untersuchungen. 2.ges. Neurol. Psychiut., 171, 167-199. R. M. E., AND GRUNDFEST, H., (1954); Electrophysiological studies of cerebellar inflow. CARREA, 1. Origin, conduction and termination of ventral spino-cerebellar tract in monkey and cat. J . Neurophysiol., 17, 208-23 8. CHAMBERS, W. W., AND SPRAGUE, J. M., (1955a); Functional localization in the cerebellum. I.

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Organization in longitudinal corticonuclear zones and their contribution to the control of posture, both extrapyramidal and pyramidal. J. cump. Neurol., 103, 105-129. CHAMBERS, W. W., AND SPRAGUE, J. M., (1955b); Functional localization in the cerebellum. 11. Somatotopic organization in cortex and nuclei. Arch. Neurol. Psychiat. (Chic.), 74, 653-680. COMBS,C. M., (1954); Electro-anatomical study of cerebellar localization. Stimulation of various afferents. J . Neurophysiol., 17, 123-143. ECCLES, J. C., HUBBARD, J. I., AND OSCARSSON, O., (1961a); Intracellular recording from cells of the ventral spino-cerebellar tract. J . Physiol. (Lond.), 158, 486-516. ECCLES, J. C., OSCARSSON, O., AND WILLIS, W. D., (1961b); Synaptic action of group I and I1 afferent fibres of muscle on the cells of the dorsal spino-cerebellar tract. J. Physiol. (Lond.), 158, 517-543. FERRARO, A., AND BARRERA, S. E., (1935); The nuclei of the posterior funiculi in Macacus rhesus. An anatomic and experimental investigation. Arch. Neurol. Psychiat. (Chic.),33, 262-275. GRANIT, R., AND PHILLIPS, C. G., (1956); Excitatory and inhibitory processes acting upon individual Purkinje cells of the cerebellum in cats. J . Physiol. (Lond.), 133, 520-547. GRANIT,R., SKOGLUND, S., AND THESLEFF, S., (1953); Activation of muscle spindles by succinylcholine and decamethonium. The effects of curare. Acta physiol. scand., 28, 134-151. GRANT,G., (1962a); Projection of the external cuneate nucleus onto the cerebellum in the cat: An experimental study using silver methods. Exp. Neurol., 5, 179-195. GRANT,G., (196213); Spinal course and somatotopically localized termination of the spinocerebellar tracts. An experimental study in the cat. Actaphysiol. scand., 56, Suppl. 193, 1 4 5 . GRUNDFEST, H., AND CAMPBELL, B., (1942); Origin, conduction and termination of impulses in the dorsal spinocerebellar tracts of cats. J . Neurophysiol., 5, 275-294. HOLMQVIST, B., LUNDBERG, A., AND OSCARSSON, O., (1956); Functional organization of the dorsal spino-cerebellar tract in the cat. V. Further experiments on convergence of excitatory and inhibitory actions. Acta physiol. scand., 38, 76-90. HOLMQVIST, B., OSCARSSON, o., AND ROSBN,I., (1963a); Functional organization of the cuneocerebellar tract in the cat. Acfa physiol. scand., 58, 216-235. HOLMQVIST, B., OSCARSSON, O., AND UDDENBERG, N., (1963b); Organization of ascending spinal tracts activated from forelimb afferents in the cat. Acta physiol. scand., 58, 68-76. LAPORTE, Y . , LUNDBERG, A., AND OSCARSSON, o., (1956); Functional organization of the dorsal spino-cerebellar tract in the cat. 11. Single fibre recording in Flechsig’s fasciculus on electrical stimulation of various peripheral nerves. Acta physiol. scand., 36, 188-203. LIVINGSTON, A., AND PHILLIPS, C. G., (1957); Maps and thresholds for the sensorimotor cortex of the cat. Quart. J . exp. Physiol., 42, 190-205. LLOYD,D. P. C., AND MCINTYRE, A. K . , (1950); Dorsal column conduction of group I muscle afferent impulses and their relay through Clarke’s column. J. Neurophysiol., 13, 39-54. LLOYD,D. P. C., AND WILSON,V. J., (1957); Reflex depression in rhythmically active monosynaptic reflex pathways. J . gen. Physiol., 40, 409426. LUNDBERG, A., AND OSCARSSON,o.,(1956); Functional organization of the dorsal spino-cerebellar tract in the cat. 1V. Synaptic connections of afferents from Golgi tendon organs and muscle spindles. Acta physiol. scand., 38, 53-75. LUNDBERG, A., AND OSCARSSON, o., (1960); Functional organization of the dorsal spino-cerebellar tract in the cat. VII. Identification of units by antidromic activation from the cerebellar cortex with recognition of five functional subdivisions. Acta physiol. scand., 50, 356-374. LUNDBERG, A., AND OSCARSSON, o.,(1962); Functional organization of the ventral spino-cerebellar tract in the cat. IV. Identification of units by antidromic activation from the cerebellar cortex. Acta physiol. scand,, 51, 252-269. LUNDBERG, A., AND WINSEURY, G., (1960); Functional organization of the dorsal spino-cerebellar tract. VI. Further experiments on excitation from tendon organ and muscle spindle afferents. Acta physiol. scand., 49, 165-170. MCINTYRE, A. K., (1962); Central projection of impulses from receptors activated by muscle stretch. Symposium on MuJcle Receptors. D. Barker, Editor. Hong Kong, University Press (p. 19-30). MOUNTCASTLE, V. B., COVIAN,M. R., AND HARRISON, C. R. (1952); The central representations of some forms of deep sensibility. Ass. Res. nerv. Dis.Proc., 30, 339-370. OSCARSSON, O., (1957a); Primary afferent collaterals and spinal relays of the dorsal and ventral spino-cerebellar tracts. Acta physiol. scand., 40, 222-23 1. OSCARSSON, O., (1957b); Functional organization of the ventral spino-cerebellar tract in the cat. 11. Connections with muscle, joint, and skin nerve afferents and effects on adequate stimulation of various receptors. Acta physiol. scand., 42, Suppl. 146, 1-107.

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OSCARSSON, O., (1960); Functional organization of the ventral spino-cerebellar tract in the cat. 111. Supraspinal control of VSCT units of I-type. Actaphysiol. scand., 49, 171-183. OSCARSSON, O., AND ROSBN,I., (1963a); Cerebral projection of Group 1 afferents in forelimb muscle nerves of cat. Experientia (Basel), 19, 206. O., AND ROSEN,I., (1963b); Projection to cerebral cortex of large muscle spindle afferents OSCARSSON, in forelimb nerves of the cat. J. Physiol. (Lond.), 169, 924-945. POMPEIANO, O., (1958); Responses to electrical stimulation of the intermediate part of the cerebellar anterior lobe in the decerebrate cat. Arch. ital. Biol., 96, 330-360. REXED,B., A N D STROM,G., (1952); Afferent nervous connexions of the lateral cervical nucleus. Acta physiol. scand., 25, 219-229, SHERRINGTON, CH. S., (1890); On out-lying nerve-cells in the mammalian spinal cord. Phil. Trans. B, 181, 3348. SHERRINGTON, CH. S., (1893); Note on the spinal portion of some ascending degeneration. J . Physiol. (Lond.), 14, 255-302. A., (1944); Receiving areas of the tactile, auditory and visual systems SNIDER, R. S., AND STOWELL, in the cerebellum. J . Neurophysiol., 7 , 331-357. WOOLSEY, C. N., (1947); Patterns of sensory representation in the cerebral cortex. Fed. Proc., 6, 437441. C. N., (1959); Some observations on brain fissuration in relation to cortical localization WODLSEY, of function. Structure and Function of the Cerebral Cortex. D. B. Tower and J. P. Schade, Editors. Proc. 2nd Int. Meet. Neurobiol. Amsterdam, Elsevier (p. 64-68). DISCUSSION

GELFAN:The cortical projection of afferent outflow from muscle, particularly in group la fibers, has interested us for some time, as it has other neurophysiologists. Since hitherto experiments on animals failed to demonstrate any such projection of impulses from spindle annulo-spiral endings, Dr. Sylvester Carter, a hand surgeon, and I decided to test it in man. So far we have tried it only on 4 suitable surgical cases, in which the tendons at the wrist were exposed under local anaesthesia, limited to the skin, and with no pre-operative medication. When a tendon was pulled so as to stretch the muscle, as for example the palmaris longus, the sensation was never referable to the muscle. The patient would sometimes report that the skin over the muscle area was being pulled. When the tendons were pulled so as to move the fingers, the reports accurately identified the specific finger movement, i.e. joint movement was readily recognized and appreciated. But there has so far been no evidence of any coiiscious recognition of changes in length of muscles. OSCARSSON: Our experiments have, so far, been limited to the cat and we don’t know anything about the organization in other species. However, the information reaching the cerebral cortex from large muscle spindle afferents in the cat might not enter the ‘consciousness’ of the animal. This is suggested by the recent investigation of Giaquinto, Pompeiano and Swett (Arch. ital. Biol., 101 (1963) 133-148). These authors showed that repetitive stimulation of group I afferents in the deep radial nerve did not influence the EEG and behaviour of sleeping or waking cats. The group I projection terminates in what is presumably the motor cortex of the cat and might represent a feedback system adjusting movements elicited from this cortical area. Thus the cerebral cortex seems to contain mechanisms as unrelated to consciousness as the motor regulating mechanisms in the cerebellum.

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CREUTZFELDT: I should like to ask Dr. Oscarsson whether he has an idea in which thalamic nucleus the corticopetal Ia afferents may be relayed. lntracellular recordings from Betz cells in the cat motor cortex performed in our lab (Lux, Nacimiento and myself) have consistently shown short latency primary EPSPs after stimulation of the VPL nucleus of the thalamus. This monosynaptic connection between VPL and Betz cells may represent the next link in a la-spino-corticospinal reflex pathway whose centrifugal path would then be the corticospinal tract. The relatively low following frequency of cortical responses may suggest a frequency limiting recurrent inhibition in the thalamic relay as assumed also in other thalamo-cortical systems. OSCARSSON: We have not investigated the site of the presumed thalamic relay. KUYPERS: The data you presented are of extreme interest to me since we have been looking at the descending pathways to the cuneate and gracilis nucleus. At least in monkey there is some precentral projection to the cuneate and gracilis. Peculiarly enough it was always thought that the cerebral projection was first and foremost postcentral and only in exceptional cases did the Woolsey school feel that there was any precentral contribution. Dr. Creutzfeldt has pointed out that the VPL projects to the precentral gyrus or an area comparable to the precentral gyrus. This would mean that the precentral gyrus is part of a VPL-circuit and this would facilitate the explanation of a projection to the cuneate and gracilis nucleus.