Somatotopic studies on red nucleus: spinal projection level and respective receptive fields.

Somatotopic Projection J. C. ECCLES,

Studies Level

on Red Nucleus:

and Respective

T. RANTUCCI,

P. SCHEID,

AND

Spinal

Receptive

Fields

H. TABOiirKOVA

Departments of Physiology and Biophysics, State University New York 14226; and Max-Planck-Institut fiir Experimentelle

of

New York, Buffalo, Medixin, Giittingen, Germany

THERE ARE SEVERAL thorough anatomical studies of the projections of the red nucleus neurons to the spinal cord of the cat, particularly with respect to the locations of these RN neurons in the red nucleus (5, 20, 26, 29, 36, 37). It was reported that these projections are virtually restricted to the caudal three-fourths of the red nucleus, the pars magnocellularis. Furthermore, it was reported that the RN neurons projecting only to the cervical level tend to lie medially and dorsally, with the lumbar-projecting neurons laterally and ventrally, though there is admixture in the transitional region. We have attempted in this paper to evaluate this somatotopic arrangement by physiological techniques. First the pars magnocellularis is explored by a number of microelectrode insertions in a transverse or longitudinal plane, and the level of projection of single RN neurons is tested by the technique of antidromic invasion. Somatotopic maps are constructed for comparison with the anatomically determined somatotopy. Second, we have made a relative assessment of the responses of these RN neurons to inputs from forelimb and hindlimb nerves and from forelimb and hindlimb cutaneous mechanoreceptors. This assessment is correlated with the level of projection in the spinal cord. A brief reference to an early stage of this investigation has been published (16).

Special consideration was given to those experiments with at least 4 microelectrode tracks in the same plane. In this category there were 66 tracks in 8 transverse planes, with a total of 133 isolated RN neurons and 28 tracks in 5 parasagittal planes, with a total of 97 isolated RN neurons. We have constructed the somatotopic plottings on the basis of all neurons that can be isolated for unitary recording along each microelectrode track. The same microelectrode was inserted in succession along several parallel tracks lying either in a transverse or an oblique parasagittal plane. The obliquity was in a ventromedial direction of loo or 20° in different experiments. The latter angle obtained in Figs. 5 and 8. As already described (9) the tracks have been identified in celloidin sections by utilizing as a guide the line of the last track that was made prominent by leaving the microelectrode in situ until after fixation. The other tracks leave a much more tenuous trace, but identification was accomplished by utilizing the clues given by the known orientations relative to the last track. The location of neurons along a track is given by the known depths of insertion below-the surface of the superior colliculus and by the micromanipulator readings for the first track. Subsequently, the manipulator depth reading was kept as a reference throughout the whole series, hence the same micromanipulator readings in the different tracks will lie on a line orthogonal to the tracks (cf. Figs. 5-S). In all cases the same microelectrode was used for the whole of a planar series.

METHODS

Correlation of spinal projection and receptive field

The somatotopic study has been applied to the responses of RN neurons reported in the previous paper in which there is an account of the general experimental procedure (17). Received

for publication

January

13, 1975.

RESULTS

level

On functional grounds it might be conjectured that RN neurons projecting only to the cervical level would be exceptionally related to inputs from the forelimb, whereas 965

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ECCLES,

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SCHEID,

AND

TABOiifKOVA

those projecting to the lumbar level would exhibit a dominance from hindlimb inputs.

By contrast, in & the hindlimb nerves had very weak excitatory-inhibitory (EI) reacEvidence for this input discrimination has tions. Taps to the forelimb pads evoked been reported by Nishioka and Nakahama excitatory-inhibitory responses matching (28) who found that inputs from the rostra1 those from nerves, but weaker. Nevertheless, and caudal zones of the body had a soma- in C, a clear response was evoked by a totopic distribution in the red nucleus 0.04-mm tap to FCP. In D, taps of 0.4 mm corresponding to the respective cervical to FT2 and FT5 gave responses virtually and lumbar projections, as provided by identical with the l.6-mm taps in C. Air-jet anatomical studies (5, 29, 36, 37). In a critistimulation to the forelimb (E) gave also a cal examination of this conjecture of foresignificant E.I response. However, in F, limb made

and an

hindlimb approximate

dominance, we have assessment of the

relative sizes of the inputs from forelimb and hindlimb nerves and cutaneous mechanoreceptors. Figures 1, 2, and 3 illustrate the manner of this assessment. Figure 1 illustrates responses of an RN neuron not projecting down to the lumbar level. It gave strong composite responsesto inputs from forelimb nerves, ISR and rSR (A). The ISR, in particular, showed a strong short-latency

excitation

plete inhibition

A

followed

by a com-

with a later strong rebound.

HCP This

degree the high specificity of input from forelimb, which matched its projection to the forelimb and perhaps the thoracic level, but not to the hindlimb cord. Because of this

/SR

both

rSR

/

/ ,,’ /:I”

/d

A...... ~/. ..

nerve

and

(HL) inputs for

mechanoreceptor

stimula-

tion, this neuron will be designated by the symbol FL 3 HL for both nerve and mechanoreceptor

inputs.

In Fig. 2A antidromic testing shows that

Nerves

2.

level of the spinal dominance of fore-

limb (FL) over hindlimb

B Forelimb

taps of 1.6 mm were without effect. neuron displayed to a remarkable

Hind

Limb

Nerves

/PER //

4.

I 20

: I

. . .-.; .7.. m.:. :. ._’ - ,‘: ...I..-d -.. =:.:. ::zr ?,.. ,r,**.r. . -. . .‘*b-.+.-,;.r’,‘. ..

I

Air

Jet Forelimb

T2

FIG. 1. Responses of RN neuron to stimulation of afferents in all four limbs. A and B show poststimulus time histograms (PSTHs) and cumulative frequency distributions (CFDs) of responses of a neuron in the right RN that were evoked by inputs from left and right superficial radial and left and right common peroneal nerves. In C are CFDs of responses of that neuron to taps to the central pad of the left forefoot at the indicated amplitudes. In D are responses to 0.4-mm taps to toes 2 and 5 of the left forefoot. E shows the CFD of the very slight EI response evoked by an air-jet stimulation at the indicated site on the left forefoot. In F is the CFD when taps of 1.6 mm were applied to the central pad of the left hindfoot. All PSTHs and CFDs were formed by addition of 64 traces of responses of a single RN neuron in 256 bins of 0.5 ms. The CFD was formed by cumulative addition of the PSTH bin counts. Same time scale throughout, and same count scale for all PSTHs. The count scale for the CFD is for a single average trace. Bars indicate times of stimuli and the broken lines show CFDs for the background rates of discharge. FT2 and FT5, forelimb toe 2 and 5, respectively; FCP, forelimb central pad.


SOMATOTOPY

A

D

Cord

Stimulation

Tap

B

1.6mm

ISR

4T

FCP

OF

RED

C

NUCLEUS

96’7

[PER

Tap

.-- ._-_-

4T

1.6mm

-’ _*

HCP

FIG. 2. Responses of RN neuron to inputs from nerves and cutaneous mechanoreceptors. In A are antidromic responses of the neuron to cord stimulation at the C, and L, segmental levels. In B are the PSTII and CFD evoked by stimulation of the left superficial radial nerve at 4 times threshold. Similarly, in C there are the PSTH and CFD for stimulation of the common peroneal nerve (arrows marking onset of first excitatory response) and also two specimen records with arrows marking time of stimulation. D and E give responses of the neuron to 1.6-mm taps to the central pads of forelimb and hindlimb, there being specimen records of the neuronal responses and of the pad taps in addition to the PSTH and the CFD. Same time and voltage scales for all specimen records. Same time and count scales for all PSTHs and CFDs, which are formed by addition of 64 traces in 256 bins of 0.5 ms each. In the specimen traces there are large spikes from two neurons, one having the diphasic configuration seen in A, and being identified by superimposed stars. This is the unit selected for counting by the computer. The selection was made by differentiation with a very brief time constant and was continually monitored by observation on the oscilloscope trace.

this RN neuron projected to the LZ level, the antidromic latent periods for CZ and L2 being 1.2 and 3.7 ms, respectively, giving a conduction velocity of 88 m/s. Correspondingly, the 1PER nerve was much stronger in its excitatory and inhibitory action (C) than the 1SR input (B). In Fig. 2C there was a composite action with an EIEI response beginning at the arrow. In I) and E, taps to pads match the nerve responses. Thus, for taps to FCP(D) there was an initial IE response closely paralleling that observed for the nerve in B. Even more remarkable is the matching of the HCP tap response to E to the nerve response in C, there being an initial I at the arrow and a later EI response. The second inhibition in E gave a total silence for a period of 12 ms. The RN neuron of Fig. 2 is designated by the symbol FL < HL for both nerve and mechanoreceptor inputs. Figure 3 also shows an RN neuron projecting to the L2 level (G), the respective latencies being 1.0 and 3.9 ms for CZ and Lc, stimulation, giving a conduction velocity of

87 m/s. In this neuron there was very strong EI action from both forelimb and hindlimb nerves in A and B, respectively. FCP taps in at 1.6 mm, C also evoke EI responses but possibly only an E response at 0.4 mm. HCP taps in F were more effective, there being again a strong EI response, almost as large as the nerve response. This EI response was also strong at 0.4-mm taps, but was small at 0.1 and doubtful at 0.04 mm. In D, air-jet stimulation of the forelimb gave an EI response of a moderate size. In E, on the other hand, a hindlimb air jet gave a large EI response that was even stronger than the tap response in F. This RN neuron is designated for nerve inputs and for cutaneous mechanoreceptor inputs by the symbols FL -h- HL and FL < HL, respectively. We have assembled our observations relating to the level of spinal projection and the relative inputs from forelimb and hindlimb nerves in Table 1A. In attempting this comparison, we use the approximate


968

A

ECCLES,

RANTUCCI,

ISR 6T

if-n” I +/

SCHEID,

rC I ._____... ..*...‘me. 2 : _._.._... I

1

.*’

...:

AND

TABORf

KOVA

B LPER 4T

. *.*,I .. 10 20ms

C

Tap FCP

./

FIG. 3. Responses of RN cell to inputs from nerves and cutaneous mechanoreceptors of the contralateral (left) forelimb and hindlimb. In A and B are specimen records, PSTHs, and CFDs of responses evoked by stimulation of the left superficial radial and peroneal nerves at the indicated strengths. In C and F are PSTHs and CFDs to taps to the central pads of the forelimb and hindlimb, respectively, at the indicated amplitudes. In D and E are PSTHs and CFDs of responses evoked by air-jet stimulation of the forelimb and hindlimb just proximal to the central pads. G shows the antidromic responses of the neuron evoked by cord stimulation at C, and L, spinal levels. All specimen records except G have same time and voltage scales and arrows mark stimuli. All PSTHSs and CFDs have same time and count scales, and bars indicate stimulus times. In the specimen traces of A and B, superposed stars identifv spikes that were selected for input into the computer for counting.

evaluation that has been illustrated in Figs. 1, 2, and 3. Table 1A shows that there was a definite tendency for neurons that do not project to lumbar level to have the FL input much stronger than the HL input (cf. Fig. l), but there were many exceptions to this rule. Similarly, neurons projecting to L2 level had, in most cases, the HL input much stronger than the FL input (cf. Fig. 2), but again there were excepTABLE 1. Relative assessment of inputs to RN neurons antidromically activated from C, level only or from C, and L, levels

Projection

to

A. Forelimb C, only C, Y and L, B. C, only C, and

FL > HL and 55 6

FL-^-HL -

hindlimb

nerve 22 17

FL

< HL

inputs

Forelimb and hindlimb cutaneous mechanoreceptor inputs 31 1 L, 4 10

16 37

2

26

tions. In between there are those neurons that had approximately equal inputs from FL and HL (cf. Fig. 3). Some of these did not project to the lumbar level, but 17 did. When projecting to the lumbar level it can be envisaged that the axons give collaterals in passing to the cervical level, in the manner demonstrated for the vestibulospinal tract (1). However, as against that plausible explanation, there are the many cases where there was approximate equality and projection was limited to the cervical level. Table 1B is laid out as in Table lA, but for the responses to forelimb and hindlimb pad taps. These responses show much more functional separation than with nerve inputs, there being only 3 medium to strong inputs from the HL to 34 Cz projecting cells. Correspondingly, L, projecting cells showed a dominance of HL inputs, but here there were 10 neurons with approximate equality and 4 with a much greater response to forelimb pad taps. These find-


SOMATOTOPY

OF

ings may be related to the statement above that the axons projecting to the L2 level may give collaterals to both forelimb and hindlimb regions of the spinal cord. Somatopic according

RED

969

NUCLEUS

both series the standard diphasic (positivenegative) potentials were recorded as the microelectrode passed through the red nucleus. In Fig. 4, similar depth profiles were used to investigate the zones of the nucleus which have axonal projections to the cervical levels only or to the L2 level as well. In interpreting these potential profiles it must be recognized that the Cz stimulus excites axons of all RN neurons projecting down the spinal cord. The discrimination is provided by the contrast with the potential profile evoked by the L2 stimulus. In Fig. 4A are a series of potential fields recorded at the sites marked at 0.25-mm

arrangement of RN neurons to level of spinal projection

Tsukahara, Toyama, and Kosaka (46) recorded the depth profile of field potentials evoked in the red nucleus by antidromic activation from the L2 and CZ spinal levels. Hongo, Jankowska, and Lundberg (21) also illustrated the profile of field potentials evoked by antidromic invasion of the red nucleus from the lower thoracic level. In

B Antidromic

Stimulation

Left

Antidromic

side

Right

ms

v

Simulation

Left

side

side

0 1 2 TmV It

mm

FIG. 4. Antidromic field potentials of red nucleus. In the diagram, two electrode tracks are shown penetrating through the right superior colliculus, SC, down to the red nucleus, RN. In A are the field potentials recorded in response to stimulation of the rubrospinal tract on the left side at C, and L, levels. Responses were recorded at 250-vrn intervals, as shown by dots on the track, and there are two identifying broken lines from two recording sites to the respective traces. Arrows in the L, series indicate the small potential fields remotely generated. In B is a similar series for the lateral microelectrode track. In three of the L, traces, arrows indicate the large antidromic field potentials. Records are formed by superposition of one, two, or three traces. Same time and voltage scales throughout.


970

ECCLES,

RANTUCCI,

SCHEID,

intervals along a microelectrode track passing through the medial zone of the red nucleus, the responses being evoked by stimulation of the rubrospinal tract at the C2 and L, levels of the spinal cord. At all sites within the red nucleus there was, with CZ stimulation, a large negative potential signaling the antidromic invasion of KN neurons. In contrast, L2 stimulation was almost ineffective, there being only small potentials (at arrows) signaling antidromic invasion of RN neurons remote from the recording site. In addition, there were two later spontaneous responses. The fields from remote recording can also be seen for the C2 responses at the five sites adjacent to the red nucleus. In Fig. 4B the microelectrode track was through the lateral zone of the red nucleus. Again there were large antidromic field potentials from the CZ stimulation at all recording sites in the red nucleus, and smaller potentials at the five sites adjacent to the red nucleus. In contrast to the medial track of A, L2 stimulation evoked large negative field potentials (arrows) at three deep recordings in the red nucleus. Thus,

B

A

AND

TABORfKOVA

the L2 potential profile indicates that there is, in the ventrolateral zone of the red nucleus, a dominant population of RN neurons with projections to the L2 level, which is in good accord with the anatomical findings (29, 37). The longer conduction time from L2 level results in considerable temof the individual antiporal dispersion dromic spike potentials. When allowance is made for this dispersion, there would appear to be almost as many units in the L2 as in the C2 responses at these three recording sites. A more analytic investigation is provided by recording from individual RN neurons along a series of microelectrode tracks lying in a transverse plane through the red nucleus. Figure 5 is a somatotopic map to show the C2 or L2 projection of 25 RN neurons that were recorded from in a unitary manner along seven microelectrode tracks in a single transverse plane across the The rostrocaudal location red nucleus. would be approximately in the center of the pars magnocellularis. With only one all the neurons on the ventroexception, lateral aspect of the red nucleus projected

89

1

.

.

.

.

*

..

0

5mm FIG. 5. Antidromic invasion of RN neurons recorded along a series of tracks in a transverse plane. A is a transverse section of mesencephalon with the microelectrode, ME, shown in the most medial position. SC, left superior colliculus; RN, right red nucleus. B is an enlargement of the red nucleus with the location of nine ME tracks numbered in time sequence, the last, 9, being that shown in A. Along tracks are located 28 RN neurons, which are shown with symbols indicating their invasion from stimulation at C, level only (filled circles) or from stimulation at both C, and L, levels (open circles). Depths are only approximately from the surface. They are derived from the depth for track 1, all subsequent values being instrumental, as described in METHODS,


SOMATOTOPY

to the LZ level and all others only to the C2 level. The exception was in track 5 close to the line of demarcation. The somatotopy revealed in this trartsverse section is in excellent accord with the anatomically determined somatotopy (26, 29, 37). Figure 6A and B are two somatotopic maps through the red nucleus in an oblique (20”) parasagittal plane, the angle being as shown for the microelectrode tracks in Fig. 5. The parasagittal plane of Fig. 6A was 0.5 mm medial to that of Fig. 6% In both these maps, there were only a few widely scattered neurons invaded antidromically from L,; four of the total of seven were in the extreme ventral zone of the red nucleus and, hence, are in accord with the histological somatotopy that is illustrated by Pompeiano and Brodal (ref 37, Fig. 24 B). It is disappointing that in Fig. 6 there were so few neurons projecting to LB. Possibly there would have been more if the parasagittal plane had been more lateral, but it was fairly lateral in Fig. 6B, because tracks as far as 1 mm medial encountered three RN neurons (not illustrated). One interesting feature of the somatotopy of Fig. 6 is the demonstration that RN neurons projecting

A Depth

OF

RED

9

.i

f

971

down the spinal cord are distributed longitudinally in the pars magnocellularis for almost 2 mm. This finding is in good accord with the anatomical somatotopy (26, 29, 37). Conrelation of receplive field neurons with location in pars magnocellularis

of

In the first section of the RESULTS it was shown that there tended to be a dominance of hindlimb inputs onto RN neurons projecting to the L2 level, while reciprocally there tended to be a dominance of forelimb input on RN neurons projecting to C2 but not to L2 levels (cf. Table 1). There were many exceptions. For example, of the neurons not projecting to LB, 38 of 93 had an input from hindlimb nerves equal to or greater than the forelimb nerve input. We can now ask the question: Do these exceptional neurons tend to be located in proximity to the L,-projecting neurons? For the purpose of somatotopic mapping of RN neurons with respect to the inputs from forelimb and hindlimb nerves we have assessed the excitatory and inhibitory responses in a scale of 3 star, 2 star, 1 star,

B 10

NUCLEUS

8

J

2

3

4

5

Depth

D

8.5-

e -D

8.5mm 9Rost. ,-

. - I1 .:.;I .

95

lo-,;I * \:*:.

.

FIG. 6. Antidromic invasion of RN neurons recorded along a series of tracks in two parasagittal planes. In A are 16 RN neurons in 5 microelectrode tracks through the red nucleus that is shown in outline. Tracks were inclined 20° from the dorsoventral axis as in Fig. 5. Same symbols as in Fig. 5; filled circles, only C, antidromic invasion; open circles, both C, and L, invasion: B: same red nucleus as in A, but for a parasagittal plane 0.5 mm more lateral, there being 26 RN neurons along five tracks. Scale shows approximate depth from surface of superior colliculus in millimeters, derived as for Fig. 5B,


972

ECCLES,

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SCHEID,

and zero, as was done for interpositus neurons (8). In Fig. 7 these assessments have been plot ted for each neuron along three tracks in a parasagittal plane, A for excitatory and B for inhibitory responses. The broken line separates the RN neurons according to their level of projection in the spinal cord, dorsally CZ only, ventrally to LZ as well. The interesting features were the dominance of FL nerve responses, both excitatory (E) and inhibitory (I), for all seven of the &-projecting neurons; and reciprocally with the 12 L,-projecting neurons there was dominance of HL nerve responses in 8 for E and in 9 for I, there being approximate equality for the remainder. Thus, with these RN neurons there was a remarkable correspondence between the level of axonal projection and the somatotopic responses. Nevertheless, almost all C2 neurons gave significant E

AND

TABORfKOVA

and I responses to hindlimb nerve inputs, and similarly for L,-projecting neurons and forelim b nerve inputs. These “aberrant” cateinputs correspo nd to the aberrant gories in Table 1A. Figures 7C and D show E and I responses evoked by taps for the neurons of track 1, which was the only track in which there was testing with toe taps. The somatotopy was remarkablestrong E and I actions from forelimb taps on all C2 neurons and zero action of hindlimb taps, and reversed somatotopy for the only L,-pro .jetting neuron. The relationship of aberrant inputs to neuronal location can be further examined in the transversely oriented tracks of Fig. 8. Again the broken line separates the Cyfrom the L,-projecting neurons in the ventrolateral zone, but there was one exception indicated by the arrow. In Fig. 84 there were three &-projecting neurons with

PAD TAPS

NERVES

A Depth 7mm

B

Excitation 1

2

3 .

1

C

Inhibition 2

3

FL HL~

Excitation 1

D 7mm

8-

Inhibition

1 Z

(::o 4;

-

j,

.

FIG. 7. Somatotopic plots in a parasagittal plane for excitatory and inhibitory responses of RN neurons to inputs by nerve and pad taps. In A are the excitatory responses of 19 RN neurons at locations shown along three tracks. Each neuron is denoted by a double symbol signifying the sizes of its responses to forelimb and hindlimb nerve inputs, as shown in the key diagram. Open circles indicate zero response. The broken line shows the demarcation between neurons antidromically invaded from C, level only, the dorsal group, and from both C, and L, levels, the ventral group. In B are the inhibitory responses for these same RN neurons. In C and D the responses were evoked by pad taps, but only neurons of track 1 are shown by the same symbols, C being the excitatory and D the inhibitory responses. Approximate depths below the surface of the superior colliculus are given in millimeters (cf. Fig. 54. The microelectrode tracks were inclined 10” from the dorsoventral axis. The outline of the red nucleus is partly shown in its dorsal and ventral boundaries.


SOMATOTOPY

NERVES

A Excitation

B

Inhibition

OF

RED

NUCLEUS

C

973

PAD

TAPS

Excitation

D

Inhibition

La 10

FIG. 8. Somatotopic plots in a transverse plane for excitatory and inhibitory responses of RN neurons to inputs by nerve and pad taps. In A are the excitatory responses of 15 RN neurons along five tracks in a transverse plane and inclined at 200 to the dorsoventral axis. The broken line shows the demarcation between neurons antidromically invaded from C, level only, the dorsomedial group, and from both C, and L2 levels, the ventrolateral group. There is one exceptional neuron (marked by arrow) below the demarcation line that had only C, invasion. Symbolic representation of neurons is as in Fig. 7. B is similar to A, but for inhibitory responses. C and D are similar to A and B, but are for excitatory and inhibitory responses evoked by pad taps, and only 10 of the 15 neurons were subjected to these inputs. Depth scale for all tracks gives approximate depth below the surface of the superior colliculus (cf. Fig. 5B).

a larger E input from hindlimb nerves and two others with approximate equality. The deepest neuron in track 2 (marked by arrow) projected only to C&, despite its location in the LZ-projection zone, and it received an E input from hindlimb nearly as large as from forelimb. Otherwise five of the seven neurons in the L2-projection zone had a dominance of hindlimb E input, there being equality in the remaining five. In Fig. 8B the I actions on C2 neurons were usually small or zero, there being forelimb nerve dominance in two and hindlimb in one. Somatotopic differentiation was better with the L2 neurons-five with hindlimb dominance and two with equality. In Fig. SC and D, the responses to pad taps were small, but displayed a more defined somatotopy for the five &-projecting neurons with four responding to forelimb taps by a larger E. However, with the five L2-projecting neurons, hindlimb taps gave larger E responses in only two, but in four were more effective in evoking I responses. In summary of Figs. 7 and 8 it can be stated that, except for Fig. 7C, D, there was no strict somatotopy with respect to the level of projection of the neurons. Never-

theless, somatotopy was more evident with taps than with nerve stimulation, as has already been indicated in Table 1. The aberrant inputs to neurons were not convincingly displayed as being more prominent in neurons close to the transitional zone between L,- and &-projecting neurons. In general, the degrees of admixture of forelimb and hindlimb inputs on RN neu1) correrons (cf. Figs. 7 and 8, and Table spond with those observed for the responses of interpositus (IP) neurons to nerve volleys and pad taps (ref 8, Figs. 2, 3, and 4 and ref 11, Table 1). Thus there appears to be little further admixture of forelimb and hindlimb inputs in the propagation from IP to RN neurons. Furthermore, there appears to be much the same tendency for nerve and pad-tap inputs to evoke large E and I conjoint responses in individual RN neurons, as was observed with IP neurons. DISCUSSION

IP to RN correlation It has now been well established by physiological and anatomical investigations that there is a fairly sharp somatotopic arrange-


974

ECCLES,

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ment of RN neurons according as they project to the lumbar or only to the cervical levels of the cord. A matching somatotopy has been described by anatomists (5, 36) for the interpositus (IP) neurons, - those receiving from the hindlimb zone of the pars intermedia, lobules 3 and 4, being rostral to those receiving from the forelimb zone, lobules 5 and 6. Unfortunately the physiologically defined somatotopy for IP neurons is much more mixed (8). In part this can be attributed to the complexi ties of the physiological inputs. To match the anatomical procedures it would be necessary to use microstimulation of the IP nucleus with recording o,f antidromic invasion of Purkinje cells. It will be appreciated that this would be an extremely laborious investigation when it is recognized that it would involve searching for the antidromically invaded Purkinje cells throughout the whole depth of the foliated cerebellar cortex. We attempted somatotopic mapping of the IP nucleus with respect to the forelimb and hindlimb inputs from nerve or from cutaneous mechanoreceptors (8). Furthermore, this was done for the inhibition of TP neurons because this is very largely a Purkinje cell action. However, even the somatotopy for inhibition did not conform with the rather strict mapping based both on anatomical data (5, 36, 47) and on physiological stimulation (24, 34, 36), where the hindlimb area with projections from lobules 3 and 4 of pars intermedia was rostral to the forelimb area of the nucleus anterior. It is remarkable, interpositus therefore, that there is a discriminative somatotopv in the red nucleus at the further stage’of transmission (Figs. 4 and 5). However, Fig. 5 depends on a new criterion, namely axonal projection level, and not on the inputs from forelimb and hindlimb nerves or cutaneous mechanoreceptors, as was done with the IP nucleus (ref 8, Figs. 2-4). In the first secti on of this paper it was found that the input somatotopy som etimes did not conform with the spinal projection level of the RN neurons (cf. Fig. 3). Table 1B shows that with cutaneous mechanoreceptor inputs there was a better correlation than with nerve inputs in Table lA, but even here there was considerable overlap,

AND

TABOfkfKOVA

particularly on the lumbar-projecting neurons. When considering the specificity of projection from IP to RN neurons, a very simple criterion can be used as a basis for comparison. The responses of interpositus and red nucleus neurons are compared in Table 2, using the criteria of Table 1 of our earlier study on interpositus neurons (11). Table 2 provides a more severe test than Table 1 for somatotopic discrimination of neurons because the criterion for being classified as forelimb only or hindlimb only is a zero response, both excitatory and inhibitory, to input from the other limb. Nevertheless, 18% of RN neurons responded exclusively to nerve volleys from forelimb or hindlimb, which is in good agreement with the 14y0 for IP neurons. With both nuclei there was, as expected, a larger specificity for responses to pad taps, but the exclusive percentage (59%) was higher for RN neurons than for IP neurons (40%). It is doubtful if this difference is significant. A lower percentage for RN neurons than for IP neurons would be expected if there were an appreciable convergence onto individual RN neurons by axons from IP neurons of the two exclusive classes, forelimb only and hindlimb only. Only the responses of our second exseries (decerebrate, unanestheperimental tized) are given in Table 2 for comparison under these same condiwith 1[P neurons tions. As would be expected, the exclusive percentages were much higher in the anesthetized RN series, 71y0 for nerves and 81% 18 and 59%, refor toe taps, as against spectively, in Table 2. 2. Exclusive responses* to ipsilateral forelimb and hindlimb inputs: decerebrate unanesthetized preparations

TABLE

No.

of neurons

Responding to Forelimb only, y0 Hindlimb only, y0 both limbs, y0 * Excitatory

and/or

127

86

272

262

13 5 82

43 16 41

6 8 86

29 11 60

inhibitory.


SOMATOTOPY

OF

In interpreting Tables 1 and 2, it must be realized that the nervous svstem is not built up in rigid categories. - When considering the control of movement from the pars intermedia of the anterior lobe to the interpositus nucleus to the red nucleus, it has to be recognized that the control of movement of a quadruped implies very fine forelimb-hindlimb coordination, and the animal must not be thought of as a fragmented automaton with forelimb inputs acting only on RN neurons projecting to the forelimb, and hindlimb inputs acting only on those projecting to hindlimb. A further discriminative test for RN neurons related to the responses evoked by taps to the toe pads of either forefoot or hindfoot. For example, in Fig. 10 of the preceding paper (17) 0.4-mm taps to all toes of the forefoot evoked almost identical responses. Such tests have been carried out on 39 RN neurons and differences of 2-star magnitude (3-l or 2-O) in the E or I responses were observed in seven neurons, i.e., in 18y0. This percentage is not significantly different from the value of 13y0 obtained for IP neurons by this test (ref 11, Fig. 6B). Since the responses of individual RI?YT neurons to inputs from nerve and cutaneous mechanoreceptors (Figs. 1, 2; ref 17, Figs. 7, 10, 11) display a discrimination between forelimb and hindlimb which is comparable with that displayed by interpositus neurons (ref 8, Fig. 1; ref 10, Fig. 2; and ref 11, Figs. 1, 2, 3), it would appear that there is a discriminative projection whereby interpositus neurons of similar receptivity tend to converge onto the same RN neurons. In the projection from interposi tus nucle us to red nucleus th ere m ust be divergence as well as the estimated convergence number of 50 (42). For example, the neuronal populations of the interpositus and the red nucleus on one side are about 10,000 and 2,000, respectively; hence, the divergence number would be about (50 X 2,000/10,000) = IO. The observed correspondence between the response patterns of IP and RN neurons provides circumstantial evidence that IP neurons with dominant HL inputs tend to project to RN neurons with lumbar projection. Reciprocally the IP neurons with dominant FL inputs tend to act synaptically

RED

NUCLEUS

975

on RN neurons with a cervical, but not a lumbar projection. This specificity of projection obtains both for the excitatory and inhibitory responses of IP neurons. In general with individual RN neurons, there tends to be a matching of large excitatory and inhibitory inputs from nerves or from cutaneous mechanoreceptors (cf. Figs. l-3, 7-9). The simplest hypothesis is that IP neurons with similar inputs tend to be congregated in colonies (8) and the neurons of a colony tend to project to the same RN neurons, so conserving the differential char acter of the responses of RN neurons with that for the reat a level comparable sponses of IP neurons. The inhibitory responses of IP neurons are conveyed to the RN neurons as a disfacilitation (43). As a first approximation the excitator y respon ses of RN neurons are attributable to the exci ta torv actions on interpositus neurons by such inputs as those from the lateral reticular nucleus and the inferior olive, and possibly other reticular inputs (1 1), while the inhibitory responses of RN neurons are attributable to Purkinje cell inhibition of IP neurons (10, 11, 43). H owever, it must be recognized that there can be a superimposed excitation of RN neurons by virtue of the disinhibitory response of IP neurons that is brought about by cessation of Purkinje cell inhibition (23). Somatotopy

of red

nucleus

We will now consider the relationship of the somatotopic observations of this paper to the many investigations on the mode of operation of the red nucleus in motor control. There is general agreement that the principal input to the RN is provided by the contralateral IP nucleus. To go back one stage earlier, Pompeiano (34) found that stimulation of the pars intermedia of the cerebellar anterior lobe caused inhibition of flexor muscles and excitation of extensors of the same side, and suggested that these actions were mediated bv a cerebellar inhibition of the IP nucleus. Stimulation of the IP nucleus usually had the reciprocal action on muscles of the same side, excitation of flexors and inhibition of extensors (35, 40), though sometimes extensors were excited (35). The latencies


97s

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SCHEID,

of excitation (lo-15 ms) and inhibition (15 ms) would conform with the suggestion that they were exerted via the red nucleus, an excitatory action on RN neurons exciting flexor motoneurons and an inhibitorv action via RN neurons that inhibit extensor motoneurons (40). There have been many studies employing electrical stimulation of the red nucleus in order to discover the mode of action of the rubrospinal tract on motoneurons. There is general agreement that the preponderant influence is excitation of flexors and inhibition of extensors of the contralateral limbs (18, 25, 33, 39, 41). Hongo, Jankowska, and Lundberg (21, 22) found that the rubrospinal tract acted on hindlimb motoneurons via interneurons, the excitatory interneurons projecting to flexor motoneurons and the inhibitory to extensor, though there was also excitation of some extensor motoneurons. These findings were in good accord with the anatomical account of the rubrospinal fibers ending in synaptic relationship to interneurons at the spinal level of their action (29). The conventional technique of stimulation gives such a diffuse excitation that, at the best, stimulations of the dorsal and ventral zones of the red nucleus are found to act on forelimb and hindlimb muscles, respectively (25, 33), which is in agreement with the anatomical findings (29, 37). Ghez (19) used microstimulation in order to secure a finer grain of discrimination. He found separate zones in the red nucleus that activated flexor, extensor, distal, or proximal muscles of a limb. These observations provide evidence for the existence of colonies of RN neurons having similar actions on motoneurons. The somatotopic to this maps of Figs. 7 and 8 lend support concept because there are zones of RN neurons with similar somatotopic inputs. The plotting of the size of excitatory and inhibitory inputs to all the neurons along a track in Figs. 7 and 8 would yield a graphical representation similar to those depicted for interpositus neurons (ref 8, of this colonial Fig. 7). The importance assemblage for effective action in the central nervous system has been discussed and illustrated (7). There is a remarkable bilaterality of

AND

TABOlkfKOVA

nerve input onto RN neurons, there being sometimes an approximate symmetry of the responses evoked by the right and left forelimb or hindlimb inputs (Fig. IA; ref 17, of input was Fig. 74. A similar bilaterality observed with the IP nucleus for both excitatory and inhibitory actions (ref 10, Fig. 2; ref 11, Fig. 4A, B). In fact, from the IP nucleus to the rubrospinal tract there is a strict channeling of the pathways with two complete decussations: first, from the IP nucleus to the RN of the opposite side; second, from the RN to the rubrospinal tract of the opposite side, i.e., to the same side as the IP nucleus. The bilateral mixing of inputs must occur earlier. In part, it occurs with the inputs to the pars intermedia, the central and rostra1 spinocerebellar tracts projecting to both sides (31). Bilateral mixing also occurs with the excitatory projections to the IP nucleus that are mediated by the bVFRT via the lateral reticular nucleus (38). Against this background of bilateral admixture in the earlier stages of the pathway-pars intermedia to IP nucleus to RN-it is surprising that the strict channeling supervenes from IP onward. Functional

role

of red nucleus

There can be no doubt that the red nucleus and the rubrospinal tract form the major channel whereby the pars intermedia of the cerebellar anterior lobe is able to exert an effective control of limb movement. Yet destruction of the red nucleus is reported to cause very little disturbance of posture and automatic movements (27). According to Chambers and Sprague (3, 4) these motor performances are under the control of the cerebellar vermis. Red nucleus destruction has a more subtle action in disturbing a wide variety of simple movements such as the placing and hopping reactions. In the attempt to understand the role of the red nucleus in movement control, Orlovsky (30) studied the responses of single RN neurons during the walking of a thalamic cat on a treadmill. A large majority of RN neurons responded in a phasic-manner during the walking. Usually there was an intense discharge during the flexor phase of each step and silence during the extensor


SOMATOTOPY

phase, which would correlate nicely with the red nucleus having an excitatory action on flexor and an inhibitory action on extensor motoneurons. However, over 20y0 showed a quite different phase relationship between the KN discharge and the step. An additional group of 17yo were unaffected by the stepping. Further investigations using such techniques as sudden brief restraints on the stepping gave complex responses. An important finding was that cerebellectomy abolished the phasic modulation of the RN neuronal discharges, but the stepping on the treadmill was virtually unaffected. In view of the powerful influence of pad receptors on RN neurons (Figs. 1, 2, 3), it can be suggested that at least some of the phasic modulation is attributable to the action of pad receptors that would be excited when the foot touches and leaves the treadmill belt. Since the pad receptors have both an excitatory and inhibitory influence on RN neurons (Figs. 1, 2, 3; also ref 18, Figs. 4, 5, and 6), many of the responses reported by Orlovsky (30) could be ascribed to the action of cutaneous mechanoreceptors excited by the stepping movements. It is important to point out that different conditions prevailed in our two experimental series. In the first, there was an intact brain with nitrous oxide anesthesia. In the second, there was a transection for decerebration some millimeters rostra1 to the red nucleus (with some sparing of the cerebral peduncles as described in Methods of ref 12) and then cessation of anesthesia. The red nucleus would thus be deprived of some of its excitatory and inhibitory inputs from collaterals of the corticospinal and corticobulbar tracts (44, 45). There was, however, no obvious difference in the RN responses between our two experimental series, but it could be suggested that the anesthetic would have depressed the cortical influences in our earlier series. Recently Padel, Smith, and Armand (32) have demonstrated a topographic projection from the motor cortex to the red nucleus in the cat. RN neurons projecting to the cervicothoracic cord received afferents from the motor cortex controlling the forelimb; whereas with RN neurons projecting to the lumbar cord, there was an input from the

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lateral part of the sigmoid gyrus. This finding leads to the hypothesis that there is an effective functional control of the red nucleus neurons by the motor cortex. The excitation of RN neurons is by collaterals from small pyramidal cells of the motor cortex, the synapses being far out on the dendrites and so, suitably placed to exert a background modulating influence (45), whereas the inhibition of RN neurons is by collaterals from large pyramidal cells, the synapses bei.ng on the somata in proximity to the synapses from the IP neurons (44). These authors have made the attractive suggestion that the two kinds of pyramidal action on KN neurons may effect a switching from cerebellar to cerebral control of the spinal motoneurons. Discharge of phasic (large) PT (pyramidal tract) cells would, by inhibi tion, weaken the cerebellorubral influence, whereas discharge of tonic (small) PT cells would strengthen it by providing an excitatory background. The recent review by Allen and Tsukahara (2) should be consulted for a critical examination of the complex field of cerebrocerebellar interaction in the control of movement, and in particular for the subtleties of interaction of the many looping circuits involved in cerebrocerebellar control of movement. Our investigations on the interpositus and red nucleus are intimately related to Fig. 6 of ref 2 in which is illustrated the circuits whereby the pars intermedia continually updates the motor cortex, and at the same time exercises a control on movement via the red nucleus that is itself also under control by the motor cortex. Cerebellar output pathway via inteypositus and red nuclei to sj9inal mfotoneurons Certain general conclusions can now be derived at the termination of our investigation on the pars intermedia of the anterior lobe (12-l 5), on the interpositus nucleus (8, 10, 1 1), and on the red nucleus was a large (ref 17 and this paper). There somatotopic mixing from the relatively discrete somatotopic responses of Purkinje cells to the inhibitory responses of the interpositus neurons, but this is not unexpected in view of the large convergence number, probably over 200. However forelimb-hind-


978

ECCLES,

RANTUCCI,

SCHEID,

limb discrimination was better preserved for the short-latency inhibitory responses (ref 8, Fig. 6). Th e excitatory interpositus responses are largely due to extracerebellar input (the lateral reticular nucleus and the inferior olive) and, as a consequence, display little somatotopic discrimination even for forelimb versus hindlimb. The pathway from interpositus to red nucleus is remarkable on two counts. First, there is no appreciable further somatotopic mixing, the forelimb-hindlimb somatotopy being not further degraded despite the convergence number of 50 (43). There is even preservation of the toe pad discrimination. Second, there is circumstantial evidence of a remarkable channeling of IP neurons with dominant forelimb inputs, both E and I, to RN neurons projecting to the cervical and not lumbar levels of the spinal cord and, complementarily but to a lesser degree, of the IP input to RN neurons projecting to the lumbar cord (Figs. 7, 8). When assessed on the relatively crude somatotopic criterion of forelimb versus hindlimb there is, therefore, a discrimination that gives the basis of a cerebellar control of forelimb and hindlimb movements. Presumably RN neurons with mixed inputs that project to L2 also may give collaterals at the cervical level (cf. ref 1) and so participate in forelimb-hindlimb coordination. A final comment is that the cerebellar circuits must not be expected to have the precision of connectivity that would be demanded for an action that was definitive and final on each movement being controlled. As conjectured elsewhere (6), cerebellar control is provisional and is continually updated by inputs from both the cerebrum and the periphery (2). SUMMARY

The somatotopic inputs into red nucleus (RN) neurons have been studied with special reference to their level of projection in the spinal cord. As inputs we employed either volleys in predominantly cutaneous nerves of forelimb and hindlimb or cutaneous mechanoreceptor discharges evoked by taps to footpads of forelimb and hindlimb. There has been physiological confirma-

AND

TABOMKOVA

tion of the anatomical findings that RN neurons projecting to the lumbar cord are located in the ventrolateral zone of the pars magnocellularis, whereas in the dorsomedial zone are RN neurons with cervical but not lumbar projection. Somatotopically there was found to be a differentiation of input to RN neurons according as they projected to the lumbar or only to the cervical cord. This finding was presented in the form both of tables and of somatotopic maps. As expected, this discrimination was more restrictive for the more selective inputs from pad taps than for nerve inputs. Nevertheless, forelimb inputs often had a considerable excitatory and inhibitory action on lumbar-projecting RN neurons, and vice versa for cervicalpro jetting neurons. There were two notable somatotopic findings that suggest specificities of connectivities. First, despite the large convergence of JP neurons onto RN neurons (about 50fold), the degree of somatotopic discrimination was about the same for interpositus and RN neurons with two testing procedures: between inputs from forelimb and hindlimb; and between inputs from pads on one foot. Second, although there was in the a considerable topointerposi tus nucleus graphical admixture of neurons with dominant forelimb or hindlimb inputs, the axonal projections of these neurons were apparently unscrambled on the way to the target RN neurons, so as to deliver the somatotopic specificities observed for two classes of RN neurons: those projecting down the spinal cord beyond L, level, and those projecting to C2 but not L,. Finally, there is a general discussion of motor control with reference to the pathway: pars intermedia of anterior lobe of cerebellum + interpositus nucleus + red nucleus + rubrospinal tract + spinal motoneurons. ACKNOWLEDGMENTS

This work was supported by a grant from tional Institute of Neurological Diseases and ROl NB0822101,2,3,4,5, and by generous support by the Dr. Henry C. and Bertha well Fund to J. C. Eccles, P. Scheid, and H. ikov5.

the NaStroke, research H. BusT;iboE-


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