Arborisation and Termination of SingleMotor Thalamocortical Axons in the Rat

T.D. AUMANN,1* J. IVANUSIC,1 AND M.K. HORNE1,2

1Department of Anatomy, Monash University, Clayton, Victoria 3168, Australia2Department of Neurology, Monash Medical Centre, Clayton, Victoria 3168, Australia

ABSTRACTThe aim of this study was to examine the arborisations and terminations of individual

thalamocortical axons in the motor system of the rat. Small, extracellular injections of ananterograde tracer (dextran-biotin) were made into the ventrolateral (VL) or ventralposterolateral (VPL) thalamic nuclei to label thalamocortical projections. Eleven motor axonsand one somatosensory axon were reconstructed through serial sections just rostral from theinjection site to their terminations in sensorimotor cortex. The smallest arbor arising from asingle motor axon extended approximately 0.9 mm rostrocaudal and 0.9 mm mediolateral, thelargest extended 3.9 mm rostrocaudal and 1.0 mm mediolateral. In some cases, two distinctplexuses of terminals were formed by an axon. In addition, motor axons formed terminals incortical layer V only or in layers I, III, and V. By contrast (and in keeping with previousreports), the somatosensory axon formed a single plexus of terminals in layer IV of the cortexthat extended approximately 0.3 mm rostrocaudal and 0.4 mm mediolateral. It is concludedthat individual motor thalamocortical neurones are in a position to influence much morewidespread cortical regions than somatosensory thalamocortical neurones. J. Comp. Neurol.396:121–130, 1998. r 1998 Wiley-Liss, Inc.

Indexing terms: motor cortex; motor thalamus; cerebellum; anatomy; histology

It has long been recognized that information concerninga particular point within a sensory receptive field isrelayed in an ordered, point-to-point manner from theperiphery through the various sensory relay nuclei to thecerebral cortex. This in turn results in a complete topo-graphical representation of the peripheral receptive organin each of its sub-cortical and cortical targets (e.g., somato-topy, retinotopy, cochleotopy). Moreover, the periphery isthought to play an instructional role in the formation ofsub-cortical and cortical sensory topography as theserepresentations develop in a sequence that begins at theperiphery and ends in the cortex, and perinatal perturba-tions of the periphery will alter these representations ateach level (for review, see Killackey et al., 1995).

What about the topography in motor systems? There is abroad topographical representation of body movement inthe primary motor cortex (Leyton and Sherrington, 1917;Penfield and Rasmussen, 1952; Woolsey et al., 1952), andthis representation is composed of individual motor effer-ent columns, some of which are responsible for the activa-tion of a single muscle or group of synergists acting about asingle joint (Asanuma and Sakata, 1967; Fetz and Cheney,1980). There are also multiple representations of a single-joint movement or individual muscle distributed overwidespread areas of the primary motor cortex (Kwan et al.,1978; Pappas and Strick, 1981a,b; Tanji and Wise, 1981;

Donoghue and Wise, 1982; Armstrong and Drew, 1984,1985; Huang et al., 1988), and intracortical microstimula-tion at a given motor cortical site often produces a mixedmovement response of different muscle groups (Armstrongand Drew, 1984; Huang et al., 1988; Lemon, 1988). Somato-topy has also been reported in the ‘‘motor’’ thalamus of theprimate (Strick, 1976a,b; Jones et al., 1979; Horne andPorter, 1980). By analogy with the somatosensory system,the motor thalamus should determine, or at least influ-ence, organisation and somatotopy within the motor cor-tex.

The aim of this study was to examine the arborisationsand terminations of individual motor thalamocortical axonsin the rat to allow comparison with published reports ofthe terminations of individual somatosensory thalamocor-tical axons in the rat (Jensen and Killackey, 1987) andother species (Landry et al., 1987; Garraghty et al., 1989;Garraghty and Sur, 1990).

Grant sponsor: National Health and Medical Research Council of Austra-lia; Grant number: 95 0751.

*Correspondence to: Dr. T.D. Aumann, Department of Anatomy, MonashUniversity, Wellington Road, Clayton, Victoria 3168, Australia.E-mail: tim.aumann@med.monash.edu.au

Received 23 June 1997; Revised 9 February 1998; Accepted 14 February1998

THE JOURNAL OF COMPARATIVE NEUROLOGY 396:121–130 (1998)

r 1998 WILEY-LISS, INC.

MATERIALS AND METHODS

Injection of tracers

Adult, male, Sprague-Dawley rats weighing between250 g and 350 g were anaesthetized with sodium pentobar-bitone (60 mg/kg, i.p.) and placed in a stereotaxic headframe. Small holes were drilled in the bone over theventrolateral nucleus (VL) on both sides of the brain. Acalibrated glass micropipette (10–20 µm outer tip diam-eter) filled with 2.5% dextran-biotin (Molecular Probes,Inc., Eugene, OR) in 0.1 M phosphate buffer, pH 7.4, wasadvanced vertically with a microdrive into VL at specificstereotaxic coordinates (Bregma 22.3 mm, lateral 2.0 mm,depth 6.0 mm below the surface of the brain; Paxinos andWatson, 1986). Injections into the somatosensory thalamicrelay nuclei (ventral posterolateral [VPL] and ventralposteromedial [VPM] nuclei) were made at specific coordi-nates (Bregma 22.3 mm, lateral 2.5 mm, depth 6.0 mmbelow the surface of the brain).

A small volume (5–25 nl) of the tracer solution wasslowly pressure injected (over 1 minute) extracellularlywith a Picospritzer (General Valve Corporation, Fairfield,NJ). This volume was calculated by measuring (with adissecting microscope) the fall of the tracer solution in theshaft of the micropipette. It was important to minimize theamount of tracer injected in these experiments in order tominimize the number of labeled thalamocortical projec-tions. A lower number of labeled projections enabled us totrace an individual arbor from section to section moreeasily and reliably without confusing it with other labeledarbors. The micropipette was left in situ for 10 minutesafter the injection then slowly withdrawn from the brainover a period of 5 minutes to minimize back tracking of thetracer.

Preparation of tissue for light microscopy

After a survival period of 7–14 days, each animalwas deeply anaesthetized with sodium pentobarbitone(60 mg/kg, i.p.) and perfused via the aorta with 500 mlof warm, heparinised 0.1 M phosphate-buffered saline,pH 7.4, followed by cold 4% paraformaldehyde in 0.1 Mphosphate buffer, pH 7.4. The brain was removed and leftovernight at 4°C in fixative plus 20% sucrose. It wasserially sectioned (50 µm thick) in the coronal plane on afreezing microtome, and the sections were processed histo-chemically according to the diaminobenzidine (DAB) proto-col detailed previously (Aumann et al., 1994). The sectionswere mounted on gelatinized slides, air dried, stained with1% neutral red, dehydrated, cleared, and coverslipped.

Data analysis

The location of each injection site was determined byusing a projection microscope to outline the micropipettetrack and the extent of spread of DAB reaction product.Thalamic nuclei were defined according to Paxinos andWatson (1986). A labeled axon was selected for reconstruc-tion in sections through the primary sensorimotor corticesipsilateral to the injection site. Once it was selected, theaxon and its branches and terminals were traced rostrallyand caudally through serial sections under a light micro-scope (103 ocular and 1003 oil objective) with a drawingtube attached. The labeled arbor was identified reliablyfrom section to section by matching surrounding bloodvessels and other labeled axons under lower power (103,253, and 403 objectives).

All methods conformed to theAustralian National Healthand Medical Research Council (NHMRC) published code ofpractice for the use of animals in research and wereapproved by the University Ethics Committee acting un-der the Australian (NHMRC) guidelines.

RESULTS

Classification of motor and somatosensorythalamocortical neurones

Reconstructed axons were classified as motor or somato-sensory according to two criteria. The first was the locationof the injection site (Figs. 1A–H, 2) within VL (motor) oreither the VPL and/or the VPM (somatosensory). Thesecond was the locations of terminals in either the primarymotor or primary somatosensory cortices. Although thesetwo areas of cortex overlap to some degree in the rat,movements evoked by low-threshold (,30 µA) intracorti-cal microstimulation correspond with the cytoarchitectur-ally defined lateral agranular (AGl) or primary motor (M1)cortex, whereas the primary somatosensory (S1) cortexcorresponds with granular (G) regions of cortex (Donoghueand Wise, 1982).

The location of terminals was important in the context ofthis study, because 1) the axonal arbors were not recon-structed fully back to their cell body of origin (the proximalportion of the axon and its cell body were obscured due tothe high density of DAB reaction product around theinjection site), and 2) the injection sites were not alwaysconfined within either somatosensory or motor thalamus.All of the arbors described as motor in the present studyterminated solely within AGl (although two terminatedalso in the medial agranular [AGm] cortex), and the arbordescribed as sensory terminated solely within G.

Motor thalamocortical projection

In total, 11 motor thalamocortical axons were recon-structed. Each of these followed a similar trajectory throughto its termination in the cortex. The reconstructions com-menced 0.4–2.0 mm rostral from the injection site, typi-cally around the point of passage through the thalamicreticular nucleus (Rt). Collateral branches and terminalsin Rt were observed for each of the axons but could not bereconstructed because of 1) their very fine nature and 2)obstruction by other anterogradely labeled Rt terminalsand by retrogradely labeled Rt cell bodies (dextran-biotinis transported in both directions). Sawyer et al. (1994)provide an excellent description of Rt collaterals andterminals in the rodent motor thalamocortical system.From Rt, the axons coursed in a rostral and lateraldirection through the internal capsule (ic), then throughthe external capsule (ec), to a point that is marked with anarrow in Figures 3A–D and 4A–C. There, they ascendedsharply into the cortex and coursed for quite some distancein a caudal direction through the cortex (Figs. 3A–D,4A–C). Indeed, one of the parent axons (not shown) wastraced as far caudal as the level of the injection site. Wecould not follow it farther, because only sections rostralfrom the injection site were collected.

Data obtained from each of the 11 motor axons aresummarized in Table 1. Once the parent axons had enteredthe cortex, they gave off numerous branches along theirlength. Each of these branches arborised farther in thehorizontal plane and formed en passant and terminaux-

122 T.D. AUMANN ET AL.

Fig. 1. Photomicrographs of the approximate center of each of theinjections sites (black reaction product) that gave rise to the sevenmotor axons (A–G) and the single somatosensory axon (H) illustratedin Figures 3A–D and 4A–D. The injection sites in C,F, and H areindicated by arrowheads. Approximate borders of different nuclei have

been outlined. AV, anteroventral; CL, centrolateral; LD, laterodorsal;mt, mammillothalamic tract; Po, posterior group; Rt, reticular; VM,ventromedial; VPL, ventral posterolateral; VPM, ventral posterome-dial; VL, ventrolateral. Scale bar 5 500 µm (applies to all).

Fig. 2. Photomicrographs of axonal and terminal labeling.A: Branching axon leading to the plexus F,G, and H in axon N8 (Fig.4B). B,C: Axon branches near points C and D, respectively in N4 (Fig.3C). D: Superficial axon and bouton (arrowhead) in layer I of the motorcortex near point G in N5 (Fig. 3D). E,F: Axons and terminal boutons(arrowheads) in layer V of the cortex near point E in N8 (Fig. 4B).

G: Axonal branching and termination in layer V of the motor cortexnear point G in N10 (Fig. 4C). H: Branches near point C in N9 (Fig.4D). The orientation of this photomicrograph is rotated 90° (counter-clockwise) relative to Figure 4D. Scale bars 5 5 µm in A,E,F, 20 µm inB,C,D, 10 µm in G, 12 µm in H.

Fig. 3. Illustrations of four reconstructed motor axons. Each arboris illustrated in detail as it appeared in the frontal plane (maindrawing) and also as a cartoon superimposed on three equally spaced(2 mm apart) frontal sections through the thalamus and sensorimotorcortices. Major points of interest are indicated by letters and corticallayers (I–VI) are indicated by dotted lines. The arrows indicate thepoints at which the parent axons altered their courses from rostral tocaudal in the external capsule or in cortical layer VI, and the questionmarks indicate branches that were not able to be reconstructed fullythrough to their end. A: Axon N2, which arose from the injectionshown in Figure 1A. The most rostral terminals were formed bybranch D in layer V of the lateral agranular cortex (AGl). BranchesC,E,F, and G formed terminals at progressively caudal locations alsoin layer V of AGl. B: Axon N3, which arose from the injection shown inFigure 1B. This axon formed at least two distinct terminal plexuses

separated by 2 mm rostrocaudally. The rostral plexus (point E) waslocated in layer V of AGl, and the caudal plexus (points F and G) waslocated in layers I, III, and V of the medial agranular cortex (AGm).Two branches (points B and C) could not be traced through to theirterminations. C: Axon N4, which arose from the injection shown inFigure 1C. This arbor was the smallest (in cortical areal terms) of allthe motor arbors reconstructed. It formed a single, localised plexus ofterminals (points C–E) within cortical layer V of AGl. D: Axon N5,which arose from the injection shown in Figure 1D. This axonappeared to be forming two distinct plexuses (rostral at points C and Eand caudal at points G and H); however, the interconnecting segmentof axon (point F) formed a number of en passant boutons in layer V.Terminals arising from this axon were located in layers I, III, and V ofAGl. Scale bars 5 200 µm (applies to the main drawing only; boutonsand axons are not drawn to scale).

Fig. 4. Illustrations of three reconstructed motor axons (A–C) andone sensory axon D. A: Axon N6, which arose from the injection shownin Figure 1E. Branches B and D were not reconstructed fully butformed terminals in layer V of rostral AGl (points C and E). The parentaxon coursed caudally and formed additional terminals in layer V ofAGl (points F, G, and H) 1.5 mm away from the rostral terminals. It isnot clear whether this axon formed two distinct plexuses of terminalsbecause of the incompleteness of the reconstruction. B: Axon N8,which arose from the injection site shown in Figure 1F. This axon gaveoff a branch at point B in the striatum that could not be traced farther.Cortical terminals were formed more or less uniformly throughoutlayer V over a very widespread area of AGl. C: Axon N10, which arose

from the injection shown in Figure 1G. This was the second axon in thesample that clearly formed two distinct plexuses of terminals. Therostral plexus (points D and E) was located in layers I, III, and V ofAGl, and the caudal plexus (points G and H) was also located in layersI, III, and V of AGl. The rostral and caudal plexuses overlapped to asmall degree. D: Axon N9, which arose from the injection shown inFigure 1H. This somatosensory axon coursed in a rostral and lateraldirection through the thalamic reticular nucleus and then through theinternal capsule to point B in the external capsule. There, it turnedand ascended laterally into the cortex, forming a number of branchesand a dense plexus of terminals in layer IV of the granular cortex(point D). Scale bars 5 200 µm.

type cortical boutons. Typically, one large plexus or twosmaller but distinct plexuses of terminals were found toarise from a single axon. Terminals were restricted largelyto AGl, although two axons (N3 and N7) formed terminalsin both AGl and AGm. The areal extent of terminals formedby each axon is indicated in Table 1 by the maximumrostrocaudal and mediolateral separation of terminals ineach plexus. Obviously, the true areal influence of eachaxon is less than these measures suggest, because 1) thearbors are not square in shape when they are viewed in thehorizontal plane, and 2) there are regions within eacharbor that are free of boutons. Nevertheless, there wasclearly a much greater degree of divergence in the motorthalamocortical pathway than in the sensory thalamocorti-cal pathway. There was also evidence of two types of motorthalamocortical axons that were distinguishable on thebasis of the laminar distribution of their terminals: onetype that terminated in layer V only and the other thatterminated in layers I, III, and V.

Sensory thalamocortical projection

In contrast to the motor axons, the sensory axon formeda single and localized plexus of terminals in layer IV ofgranular cortex (Fig. 4D, Table 1). The density of corticalboutons arising from this somatosensory axon was muchgreater than for any of the motor axons, confirmingprevious findings in the cat (Asanuma et al., 1974; De-schenes and Hammond, 1980). The rationale for recon-structing this somatosensory thalamocortical axon was tocompare our method with intracellular or intraaxonalinjection of a neuroanatomical tracer. By using this lattermethod, a number of studies have shown that the terminalarbors of somatosensory thalamocortical neurones typi-cally lie within a localized area of cortex and are restrictedto layers III and/or IV in rat (Jensen and Killackey, 1987),cat (Landry et al., 1987), and monkey (Garraghty et al.,1989; Garraghty and Sur, 1990). Our finding is consistentwith these previous studies. There are examples of farmore widespread somatosensory arborisations in the cat(Landry et al., 1987) and monkey (Garraghty and Sur,1990), but these are in the minority.

DISCUSSION

Divergence in the motorthalamocortical projection

This study demonstrates that, in the rat, individualthalamocortical neurones in the motor system arboriseand terminate over a wide cortical territory. An importantmethodological consideration concerning the interpreta-tion of these findings is the incompleteness of the recon-structions. We were unable to trace some branches throughto their end reliably because of a diminution in intensity oflabeling and/or the close proximity of labeled axons andterminals from other thalamocortical neurones. Neverthe-less, we emphasize that the true degree of divergence ofmotor thalamocortical axons can only be greater than thatdescribed in this report.

Our review of the literature, together with the datapresented here, leads us to conclude that there is typicallymore divergence at the thalamocortical level in the motorsystem than in the somatosensory system in the rat andcat (e.g., see Strick, 1973; Asanuma et al., 1974; Deschenesand Hammond, 1980; Shinoda et al., 1985b; Jensen andKillackey, 1987; Landry et al., 1987; Kakei et al., 1988;Shinoda and Kakei, 1989). Shinoda et al. made intracellu-lar recordings from cat thalamocortical neurones andfound that about 40% of their sample was antidromicallyactivated from three or more sites in the motor cortex thatwere separated from one another by 1.5–2.0 mm. Thisfinding was further investigated anatomically by intraaxo-nal injections of horseradish peroxidase (HRP) into physi-ologically identified motor thalamocortical neurones. Indi-vidual axons were reported to divide repeatedly intonumerous branches and to form two to eight separateclusters of terminals in the motor cortex. Each clusterextended 0.3–1.5 mm, and the total extent of influence ofone of these axons measured 5.0 mm rostrocaudally and4.8 mm mediolaterally (Kakei et al., 1988; Shinoda andKakei, 1989). In addition, Strick (1973) has shown that,following small lesions in the motor thalamus of the cat,degeneration is observed in a remarkably large region ofthe primary motor cortex. In contrast, small lesions in thesomatosensory thalamus result in a very focal cluster of

TABLE 1. Summary Data From All of the Axons Reconstructed

Axonnumber

Rostralor caudalinjectionin VL1

Numberof distinctterminalplexuses

Areal extent ofterminal plexus (µm)

Cortical regions in whichterminals were found

Cortical layers in whichterminals were found

RC ML AGl AGm G I III IV V

N22 Middle 1 1,400 1,800 1 1N3 Caudal 2 1,000 800 1 1

1,000 1,000 1 1 1 1N4 Rostral 1 900 900 1 1N5 Middle 1 2,000 1,800 1 1 1 1N6 Rostral 1 2,800 950 1 1N8 Rostral 1 3,900 1,000 1 1N10 Middle 2 1,600 720 1 1 1 1

850 1,350 1 1 1 1N73 Caudal 2 2 2 1 1 1 1N1 2 2 2N11 2 2 2N12 2 2 2N94 1 300 400 1 1

1VL, ventrolateral nucleus of the thalamus; RC, rostrocaudal; ML, mediolateral; AGl, lateral agranular cortex; AGm, medial agranular cortex; G, granular cortex.2Of this first group of seven motor axons, N4 was the only one that was reconstructed completely (see Figs. 3A–D and 4A–C). Therefore, the terminal data for the remaining six axonsmay be underrepresented.3Three of the four motor axons from this group (N1, N11, and N12) were reconstructed to a point just before they began forming boutons. They have been included because the degreeof preterminal branching was similar to each of the other motor axons. A few terminals on N7 were reconstructed, and their locations are indicated.4Somatosensory axon (see Fig. 4D).

MOTOR THALAMOCORTICAL NEURONES 127

degeneration in the primary somatosensory cortex. Al-though some somatosensory thalamocortical afferents inthe cat do form multiple, discrete patches of corticalterminals (Landry et al., 1987), they still appear to occupya considerably smaller cortical area than those in themotor system.

The present findings provide an anatomical basiswhereby individual motor thalamic neurones could influ-ence the activity of cortical neurones that control differentmuscles acting about different joints. It is equally possible,however, that the multiple and widespread motor thalamo-cortical projection reflects the multiple and widespreadrepresentation of individual muscles in the motor cortex(Kwan et al., 1978; Pappas and Strick, 1981a,b; Tanji andWise, 1981; Donoghue and Wise, 1982; Armstrong andDrew, 1984, 1985; Huang et al., 1988). Indeed, electricalmicrostimulation of the motor thalamus has been shown toevoke movements predominantly restricted to a singlejoint in awake monkeys (Strick, 1976b; Anner-Baratti etal., 1986; Buford et al., 1996; Vitek et al., 1996) and cats(Asanuma and Hunsperger, 1975). The functional extent ofinfluence of single motor thalamocortical neurones will bean important area of study for the future, particularly withrespect to current ideas concerning the development oftopography in the motor system raised in the introduction.

The question of whether individual motor thalamocorti-cal neurones can influence multijoint movements is alsointeresting in terms of cerebellar function. The majorafferent input to VL comes from the deep cerebellar nuclei(Yoshida et al., 1966; Faull and Carman, 1978; Schell andStrick, 1984; Shinoda et al., 1985a,b; Wiesendanger andWiesendanger, 1985). We have previously shown by usingthe same technique described in the present study thatabout 50% of individual cerebellothalamic axons arboriseand terminate over extensive areas of VL in the rat(Aumann and Horne, 1996). Shinoda (1987) has brieflydescribed similar findings in the cat. We believe that this isindicative of a capacity for some cerebellar output neu-rones to influence the activity of complex movements aboutmany joints. If VL neurones do project to multiple corticalrepresentations of the same muscle, then the corticalextent of influence (in terms of number of joints) ofindividual cerebellar nuclear neurones would be deter-mined solely by the degree of divergence in the cerebello-thalamic pathway. This notion is consistent with previousfindings that single-joint movements are typically evokedby microstimulation of the motor thalamus (Asanuma andHunsperger, 1975; Strick, 1976b; Anner-Baratti et al.,1986; Buford et al., 1996; Vitek et al., 1996), whereasmultijoint movements are a feature of cerebellar nuclearmicrostimulation (Schultz et al., 1976, 1979; Rispal-Padelet al., 1981; Cicirata et al., 1989; Ekerot et al., 1995). Itmust be stressed, however, that the cerebellothalamocorti-cal pathway was ruled out as the mediator of thesecerebellar stimulation effects in most of these studies(Schultz et al., 1976, 1979; Cicirata et al., 1989; Ekerot etal., 1995). The only cerebellar-evoked movement deficitthat has been reported after motor cortical ablation con-sisted of distalmost forelimb movements (Cicirata et al.,1989).

Cortical laminar distribution of motorthalamic terminals

We found anterogradely labeled terminals distributedthroughout layers I, III, and V, confirming previous reports

of studies in the rat (Jacobson and Trojanowski, 1975;Herkenham, 1980; Yamamoto et al., 1990). The situationappears to be much the same in the cat, although thedensity of the projection to layer V in this species appearsto be diminished considerably relative to the rat (Asanumaet al., 1974; Strick and Sterling, 1974; Deschenes andHammond, 1980; Shinoda and Kakei, 1989; Shinoda et al.,1993a,b).

Moreover, we could distinguish two groups of thalamocor-tical projections on the basis of differences in their laminardistribution of terminals. One group terminated in layer Vonly, and the other terminated in layers I, III, and V. It ispossible that we missed terminals in layers I and IIIbecause of the inability to trace all branches or incompletefilling of neurones with tracer. However, the one axon thatwe were able to reconstruct fully terminated solely in layerV, and the conditions under which this axon was labeledand prepared for reconstruction were identical to those forother axons that were found to project to layers I, III, andV. On this basis, we conclude that there are two types ofmotor thalamocortical neurones in the rat that are distin-guishable on the basis of the laminar distribution of theirterminals.

Shinoda et al. (1993b) also concluded that at least twodifferent motor thalamocortical projections exist in the cat:one that projects solely to layer III and another thatprojects to layer I. However, their conclusion was based ona comparison of one experiment in which an intraaxonalinjection of HRP labeled terminals in layer III withanother experiment in which a small population of tha-lamic neurones was labeled, and terminals were observedin layers I and III. It could have been concluded equallyfrom this that the projection to layer I also terminated inlayer III. Shinoda et al. also reasoned that the moresuperficially projecting thalamocortical axons were finer,because none of these was penetrated in the intraaxonallabeling experiment. We found no evidence for this in thepresent study. However, the two motor axons (N3 and N7)that projected to both AGl and AGm were noticeably thickerin appearance than those that projected to AGl only.

Similarly, two groups of cerebellar-receiving thalamocor-tical neurones project to the parietal cortex in the cat(Kakei and Shinoda, 1990; Wannier et al., 1992). Oneoriginates from the dorsomedial or rostral part of VA-VLand projects to layer I of the suprasylvian gyrus, the otheroriginates from the ventrolateral or caudal part of VA-VLand projects to layers I, III, and IV in the bank of theansate sulcus. We also noted that injections placed ros-trally in VL labeled axons projecting to layer V only,whereas caudal VL injections labeled axons projecting tolayers I, III, and V. Injections between these extremesresulted in labeling of both types of axons.

Although it is a speculative point, these two types ofmotor thalamocortical projections might underlie a differ-ence in afferent connectivity of the motor thalamus. Themain afferent input to VL, as mentioned above, arises fromthe deep cerebellar nuclei. It has been thought for manyyears that the dentate and interpositus cerebellar nucleiare involved in different aspects of motor control (Eccles,1969; Allen and Tsukahara, 1974). Indeed, we have al-ready demonstrated that interpositus projects to rostralVL, and dentate projects to caudal VL in the rat (Aumannet al., 1994). Given the topographical differences in thecells of origin of the different thalamocortical projectionsfound in the present study (discussed above), it is possible

128 T.D. AUMANN ET AL.

that interpositus projects to cortical layer V only (via VL)and that dentate projects to layers I, III, and V. Also,neurones with different patterns of sensory receptive fieldshave been identified in the motor thalamus of primates(Horne and Porter, 1980), and there may be a differentialdistribution of receptive field types (cutaneous vs. deep) inthe motor cortex of monkeys (Tanji and Wise, 1981) andcats (Pappas and Strick, 1981a). It is possible that thedifferent types of motor thalamocortical projections under-lie these apparent functional differences.

ACKNOWLEDGMENTS

The authors acknowledge the assistance of Sue Mitchellin preparing the photomicrographs.

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