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. 1999 Jan 15;514(Pt 2):551–566. doi: 10.1111/j.1469-7793.1999.551ae.x

Topographical organization of projections to cat motor cortex from nucleus interpositus anterior and forelimb skin

Henrik Jörntell 1, Carl-Fredrik Ekerot 1
PMCID: PMC2269074  PMID: 9852335

Abstract

  1. The activation of the motor cortex from focal electrical stimulation of sites in the forelimb area of cerebellar nucleus interpositus anterior (NIA) was investigated in barbiturate-anaesthetized cats. Using a microelectrode, nuclear sites were identified by the cutaneous climbing fibre receptive fields of their afferent Purkinje cells. These cutaneous receptive fields can be identified by positive field potentials reflecting inhibition from Purkinje cells activated on natural stimulation of the skin. Thereafter, the sites were microstimulated and the evoked responses were systematically recorded over the cortical surface with a ball-tipped electrode. The topographical organization in the motor cortex of responses evoked by electrical stimulation of the forelimb skin was also analysed.

  2. Generally, sites in the forelimb area of NIA projected to the lateral part of the anterior sigmoid gyrus (ASG). Sites in the hindlimb area of NIA also projected to lateral ASG and in addition to a more medial region. Sites in the face area of NIA, however, projected mainly to the middle part of the posterior sigmoid gyrus (PSG).

  3. For sites in the forelimb area of NIA, the topographical organization and strength of the projections varied specifically with the cutaneous climbing fibre receptive field of the site. The largest cortical responses were evoked from sites with receptive fields on the distal or ventral skin of the forelimb.

  4. Microelectrode recordings in the depth of the motor cortex revealed that responses evoked by cerebellar nuclear stimulation were due to an excitatory process in layer III.

  5. Short latency surface responses evoked from the forelimb skin were found in the caudolateral part of the motor cortex. At gradually longer latencies, responses appeared in sequentially more rostromedial parts of the motor cortex. Since the responses displayed several temporal peaks that appeared in specific cortical regions for different areas of the forelimb skin, several somatotopic maps were seen.

  6. The cerebellar and cutaneous projections activated mainly different cortical regions and had topographical organizations that apparently were constant between animals. Their patterns of activation may constitute a frame of reference for investigations of the functional organization of the motor cortex.

The cerebellar nucleus interpositus anterior (NIA) is innervated by Purkinje cells in the C1, C3 and Y zones (see Garwicz & Ekerot, 1994). In the C3 zone, climbing fibres with similar cutaneous receptive fields terminate in narrow longitudinal microzones (Ekerot et al. 1991). In NIA there is a corresponding topographical organization due to the convergence on common nuclear cell groups (sites) from Purkinje cells belonging to the same microzone. Purkinje cells within a microzone are synchronously discharged when their afferent climbing fibres are activated by natural stimulation. The resulting large positive field potentials in NIA, which reflect Purkinje cell inhibition, make natural stimulation a useful technique to identify the cutaneous climbing fibre receptive fields of nuclear sites (Garwicz & Ekerot, 1994).

For the cerebellar system comprising NIA and the C1, C3 and Y zones, all investigated afferent and efferent connections show specific relationships to the cutaneous receptive fields of climbing fibres. In the C3 zone, there is an overlap in the topographical organization of peripherally activated mossy and climbing fibre input (Ekerot & Larson, 1980; Garwicz et al. 1998) and the muscle afferent input to single climbing fibres is from muscles with specific relationships to the cutaneous receptive field of the climbing fibre (Jörntell et al. 1996). When identified sites in the forelimb area of NIA are electrically microstimulated, there is a specific relationship between their climbing fibre receptive fields and the movements evoked through the rubrospinal tract (Ekerot et al. 1995). In most cases the movement evoked at the joint just proximal to the receptive field withdraws the receptive field from an external stimulus, whereas simultaneous, more proximal movement components produce a generalized shortening of the limb.

In the cat, the cerebral projections from the cerebellar nuclei are mainly to the anterior sigmoid gyrus (ASG) of the frontal motor cortex and to the parietal cortex (see Sasaki et al. 1973). Further studies have shown that the different cerebellar nuclei exhibit gross topographical differences in their projections to ASG (Rispal-Padel & Latreille, 1974; Shinoda et al. 1985). Stimulation of cutaneous nerves activates mainly the caudolateral part of the motor cortex (Oscarsson & Rosén, 1966), a region which is largely non-overlapping with that receiving cerebellar input. The differential cortical terminations of the two afferent sources appear to correspond to gross regional differences in motor cortical function. Thus, the region receiving cerebellar input is the major origin of cortical efferents to an important precerebellar relay, the lateral reticular nucleus (Brodal et al. 1967). This region also contains the main proportion of neurons contributing to the uncrossed dorsolateral and the crossed and uncrossed ventromedial corticospinal tracts (Armand & Kuypers, 1980). The same region additionally shows special characteristics for other functional indicators, such as the timing of neuronal modulation in relation to the onset of muscle contraction (Vicario et al. 1983) and the spinal laminae of termination of corticospinal fibres (Martin, 1996).

The present study aimed to elucidate the detailed topographical organization of responses evoked in the motor cortex from the cerebellar nucleus interpositus anterior, and to describe their relationship to the distribution of peripherally evoked activity. The study focussed on the cortical projections from sites in the forelimb area of NIA and on the input from different areas of the forelimb skin.

Preliminary presentations of the results have been given (Jörntell & Ekerot, 1995, 1996).

METHODS

Preparation

Sixteen adult cats were anaesthetized with pentobarbitone (40 mg kg−1i.p., 1.5-2 mg kg−1 supplementary doses i.v. as required, usually twice per hour). The level of anaesthesia was characterized by constricted pupils and a stable blood pressure that did not respond to noxious stimulation. Cannulas were inserted into the trachea, the right cephalic vein and the right femoral artery and vein. In order to obtain stable recording conditions, a bilateral pneumothorax was made and the animals were paralysed with alcuronium in doses of about 0.5 mg h−1. The cats were artificially ventilated. The end expiratory CO2 concentration, mean arterial blood pressure and rectal temperature were monitored and kept within physiological limits throughout experiments. A continuous infusion of glucose in buffered Ringer solution was given and incisions in the skin were infiltrated with 5 % lignocaine (lidocaine). After the preparation, EEG activity was continuously monitored on an oscilloscope to keep track of the level of anaesthesia. Note that stable responses as described in the Results section required so deep an anaesthetic level that spindle-like activity was infrequent.

Craniotomies were made above the left occipital and right frontal lobes. Following resection of the left occipital lobe, the cortex of the left cerebellar anterior lobe was exposed by removing the overlying bony tentorium and the dura mater. The cerebral exposure was centred around the lateral end of the cruciate sulcus and included most of area 4γ whereas areas 6aβ, 3a and 3b were exposed to various extents. In order to increase mechanical stability a hole in the dura mater of the caudal brainstem was made. Exposed areas of the brain were prevented from drying by agar pools filled with paraffin oil.

Stimulation and recordings

Several pairs of percutaneous needle electrodes were inserted into the skin of the left forelimb (see Fig. 8A for locations). Additional percutaneous electrodes were inserted on the left half of the face (infraorbitally), across the plantar part of the left hindlimb and across the paw of the right forelimb. Stimulation parameters for the peripheral stimulation sites were a 2 mA single shock stimulus with 100 μs pulse width and 3 s interstimulus interval. A glass-coated tungsten microelectrode (exposed tip 100-200 μm) was inserted vertically to the Horsley-Clarke plane into the left half of the cerebellum in order to reach one of the cerebellar nuclei. In the cerebellum, characteristic field potentials are evoked by the percutaneous electrical stimulation used and hence the borders between white matter and the different nuclei could be identified. For the forelimb area of NIA it has been shown that sharp positive field potentials reflect the inhibitory synaptic action on nuclear neurons by climbing fibre activated Purkinje cells (Garwicz & Ekerot, 1994). By recording these field potentials to manual tactile and nociceptive cutaneous stimulation it was possible to map the climbing fibre receptive fields of the afferent cerebellar cortical microzones at different sites within the nucleus. After establishing the receptive field of a nuclear site, the electrode was connected to a stimulator. All results were obtained by stimulating sites with a 30 μA double shock (0.5 ms pulse width, 3 ms pulse interval, 3 s interstimulus interval) unless otherwise stated. All response latencies refer to the first shock. Evoked field potentials on the cortical surface were recorded with a ball-tipped surface electrode (tip diameter approximately 0.2 mm). Records of two to five sweeps with 10 ms pretrigger time and 51.2 ms total length were digitized at 50 μs and stored on a computer for off-line analysis. The band width of the recording equipment was 1 Hz (due to a high-pass filter) to 20 kHz.

Figure 8. Isopotential maps of cortical responses evoked on peripheral stimulation.

Figure 8

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A, isopotential maps of response amplitudes at latencies indicated on top left of each map for peripheral stimulation sites shown to the left. Area 4γ and cortical exposure are outlined in all maps; recording points are shown in the top left map only. Triangles indicate illustrated recording point in area 3b; stars indicate illustrated recording points for different temporal peaks in area 4γ. As a reference to the NIA projection, the projection focus of a IIIb site is indicated by a square. Single isopotential lines are drawn for responses evoked from the stimulation sites on the face and hindlimb in the maps. B, sample recordings.

In each experiment, the surface field potentials evoked from cerebellar nuclear sites and peripheral stimulation sites were recorded from a set of 50-80 cortical points in the right pericruciate cortex. These points were indicated on a photograph of the cortical exposure so that the same set of points could be recorded from throughout an experiment. The recording points were transferred to a two-dimensional coordinate system as was the outline of the exposed cortical area and the cruciate sulcus. Isopotential lines were then calculated for the field potentials evoked using the Kriging algorithm in Surfer for Windows (C) version 6.0 (see user's manual for references; Golden Software, Inc., Golden, CO, USA). Note that the presence of the cruciate sulcus could not be compensated for during these calculations. Furthermore, because of the pronounced arching of the pericruciate gyrus rostrally and laterally the distances between recording points in the extreme parts of these regions are bound to be compressed in the two-dimensional representation used.

Field potentials evoked from cerebellar nuclear sites were recorded in the depth of the cerebral cortex with a glass-coated tungsten microelectrode (approximately 50 μm exposed tip, 1 MΩ impedance at 100 Hz). The microelectrode was inserted approximately at a perpendicular angle to the cortical surface rostral to the cruciate sulcus. The electrode was advanced into white matter before recordings were made on the way back to the surface. Any mismatch in the electrode driver counter when the surface was reached again as compared with the time of insertion could then be compensated. Recording intervals were between 100 and 250 μm and the measured potentials were used to construct isopotential maps as described above. Simultaneously, surface responses near to the insertion point of the microelectrode were recorded and hence depth responses that were obviously affected by temporary changes in excitability could be excluded. The location of current sinks and sources were routinely analysed for all depth recordings by using one-dimensional current source-density analysis (CSD analysis). The theoretical basis, inherent assumptions and previous experimental implementations have been reviewed by Mitzdorf (1985). In short, the differences in voltage between recordings (average of 3 or 5 sweeps) obtained at sequential depths along single tracks were calculated in two rounds for each time bin. Thus, the second derivative of voltage against depth, a measure of the local current sink/source, was obtained.

Histology and superimposition of isopotential maps

At the end of the experiment the animal was killed with an overdose of barbiturate and subsequently perfused with formalin (10 %) in saline. The cerebellum and the frontal lobe were removed and saved for histological reconstruction of electrode tracks. As a standard procedure for the cerebellar microelectrode tracks, the depth of the most ventral Purkinje cell layer, the dorsal and ventral borders of NIA and the nuclear recording sites were noted during the experiments. Therefore, shrinkage due to the histological procedure could be compensated for when the location in NIA of a site was to be determined on frontal sections in which the electrode track had been histologically identified. In the majority of the frontal lobes, no microelectrode tracking was performed. Instead, at some selected surface recording points, pins were pushed into the cortex before sagittal sectioning to determine the relationship between cortical recording points and the cytoarchitectonic areas of Hassler & Muhs-Clement (1964).

To evaluate similarities in response topography between sites, isopotential maps from different experiments were superimposed. To this end, the cytoarchitectonic border of area 4γ was drawn on the two-dimensional coordinate systems used for construction of the isopotential maps. The outlines of area 4γ and the cruciate sulci for the different experiments were then superimposed after some rescaling (guided by photographs taken from different angles with millimeter scales attached to the brain). The outlines of area 4γ were superimposed to the best fit which always resulted in the tips of the cruciate sulci (as defined at the surface through the microscope) coinciding spatially despite differences in their trajectories from the mid-line (cf. Pappas & Strick, 1981). The border between areas 4γ and 6aβ was difficult to locate precisely in our sagittally sectioned material.

The experimental procedures were approved by the local Swedish Ethical Committee.

RESULTS

Stimulation parameters and responses evoked in the motor cortex on stimulation of cerebellar nuclei

Figure 1 illustrates the general characteristics of the extracellular field potentials recorded from the surface of the motor cortex. Responses were evoked from a site in NIA identified by the cutaneous climbing fibre receptive field of the Purkinje cells innervating the site (Fig. 1B (see Methods), nuclear location in Fig. 1C). In the deep barbiturate anaesthesia maintained throughout experiments, the baseline voltage at the cortical surface showed little variation and cerebellar-evoked responses were easily recognized (Fig. 1D). With single shock stimulation the initial positive deflection usually started at about 5 ms and was followed by a negative deflection after an additional 5-15 ms. A second shock added to the positivity already at 2 ms whereas a third shock appeared to boost neither amplitude nor rise time. Lowest thresholds were generally found to be below 2 μA. Increased stimulation intensities produced rapidly growing response amplitudes but only up to a certain level. Once this level had been attained, increased stimulation intensity mainly made the trailing negativity cut short progressively earlier parts of the positivity, resulting in a decreased latency to peak (Fig. 1D). This ‘saturation’ phenomenon was attained at about 30 μA for sites with large projection amplitudes (Fig. 1E). Response amplitudes increased with increased pulse width up to 500 μs (Fig. 1F; tested between 100 and 1000 μs for two different sites in one experiment). Stimulation parameters used for the systematic investigations (see Methods) were thus relatively efficient in producing strong cortical activation at low current intensities. Data shown in Fig. 1G and H provided clues to the cortical generation of responses. The peak positivity and peak negativity showed a strong correlation over a wide range of response amplitudes (Fig. 1G). Their strong co-variation was further indicated by their simultaneous disappearance during occasional sudden changes in excitability which left only a small, initial component of the response (Fig. 1H I). Within less than a minute, a small supplementary dose of barbiturate brought the response back to its normal configuration (Fig. 1H II). Subtraction of record I from II showed that the truncated response was entirely responsible for the initial part of the normal response (Fig. 1H III) and hence probably reflected the thalamocortical EPSP. The initial EPSP thus apparently elicited the remainder of the response in an all-or-nothing fashion.

Figure 1. Characteristics of cortical responses evoked on stimulation of cerebellar nuclear sites and the effect of altering electrical stimulation parameters.

Figure 1

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A, location in the right pericruciate cortex of recording point (star) illustrated in D, E and G. Dashed lines demarcate cytoarchitectonic areas as defined by Hassler & Muhs-Clement (1964). B, cutaneous climbing fibre receptive field of the NIA site stimulated in D, E and G (location in NIA indicated by square in C). Light and dark shading indicate extent and sensitivity centre of the receptive field, respectively. ‘Ie’ refers to the receptive field classification in Fig. 4. C, standardized frontal sections of NIA used to indicate location of NIA sites in this and following figures. D, cortical responses evoked with electrical stimulation parameters indicated to the left and on top. E, stimulus intensity plotted against response amplitude. F, effect of increasing pulse width. Single shock (50 μA) stimulation. G, peak positivity plotted against peak negativity for averages of responses in D. Symbols as in E. H, disappearance of all but the initial part of response (I) was relieved by a small dose of barbiturate (II). Record III was obtained by subtracting record I from II. Thick dashed vertical line drawn for reference. Double shock (30 μA) stimulation. F and H, two different experiments. Calibrations in H apply to D and F. r, rostral; c, caudal; m, medial; l, lateral; cor, coronal sulcus; pcd, postcruciate dimple; cruc, cruciate sulcus; NIP, nucleus interpositus posterior.

Figure 2 illustrates the surface field potentials evoked in the motor cortex on stimulation of different positions along a single microelectrode track through NIA. The cortical recording point was located where maximal response amplitudes were evoked from a NIA site with a ventral receptive field (8.00 mm, receptive field indicated at bottom left). Large responses at the selected cortical recording point were evoked only from the identified NIA site and the ventralmost NIA site, the latter of which on coarse receptive field mapping was also found to have a ventral receptive field. Coarse receptive field mapping indicated that the three dorsal NIA sites had, respectively, distal, proximal ulnar and proximal ulnar receptive fields (from ventral to dorsal). Beneath the ventral border of NIA (located at 8.80 mm) response amplitudes dropped rapidly (the area ventral to NIA was investigated for this track only).

Figure 2. Cortical responses evoked from electrode track through NIA.

Figure 2

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Thick grey line represents outline of area 4γ and the cruciate sulcus. The cortical recording point (indicated by a star) was located in the projection focus (see below) of the NIA site with receptive field indicated at bottom left. Crosses indicate stimulated sites along microelectrode track through NIA (thin outline in the middle of figure, see key in Fig. 1C). Radii of empty circles are proportional to the amplitudes of the evoked cortical responses shown to the right (stimulus intensity, 50 μA; shock artefacts truncated by the graphing software).

Generation of cortical responses evoked from cerebellar nuclei

For three NIA sites (all classified to subgroup Ia, see below) in different experiments, the depth distribution of evoked potentials in area 4γ was investigated. Figure 3 illustrates part of one experiment. The surface distribution of the evoked cortical responses is represented by isopotential maps obtained by measuring the potentials at three different latencies (see Methods and below) to give a reference for the insertions of the microelectrode. Depth recordings were analysed at several latencies between 7.5 and 23.5 ms, the first of which corresponded to the initial response component (barely visible in Fig. 3C, see Fig. 1H). The maximal negative responses occurred at a depth between 0.60 and 1.00 mm perpendicularly from the surface, i.e. in the deep part of layer III (Fig. 3D). CSD analysis indicated that distinct current sinks lasting about 20 ms were confined to a single depth between 0.60 and 0.90 mm. In a few cases, the sink of the late part of the response occurred at a slightly more superficial depth (up to 0.50 mm). Thus, despite the fact that part of the response was surface negative it was found to be entirely generated by an excitatory process in layer III. Since one-dimensional CSD analysis in essence only gives the depth(s) at which maximal second spatial derivatives of the response amplitudes occur, these results can be deduced by assessing the vertical density changes of the isopotential lines in Fig. 3D. Although not actively sought after, unit activation was usually recorded in the latency range of 10-20 ms, primarily at depths between 0.50-1.50 mm, corresponding to layers III and V.

Figure 3. Field potentials evoked in the depth of the cortex on stimulation of a NIA site.

Figure 3

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A, isopotential maps of responses evoked at the surface. Potentials were measured at the fixed latencies indicated in the top left corner of each map. Insertion points of microelectrode tracks are indicated by circles numbered from 1 to 7. Area 4γ and the cortical exposure are outlined by semithick lines. The climbing fibre receptive field of the stimulated site, its classification and its location in NIA (see key in Fig. 1C) are shown to the right. B, key to D. Microelectrode tracks are indicated in a schematic sagittal section of the motor cortex (see A). Continuous line indicates border between layers I and II; dashed line indicates border between layers III and V. Thin horizontal lines indicate depths as in D. C, recordings from one track. Thick dashed lines indicate latencies illustrated in D. D, isopotential maps of amplitudes measured at the latencies indicated in top left corner of each map. Recording points were separated vertically by 250 μm or less. Empty circles indicate track insertions; arrowheads indicate track illustrated in C. Open bars indicate the cruciate sulcus as in B. PSG, posterior sigmoid gyrus.

Outside the area of ASG where surface positivities were recorded (see Fig. 3A) and in the entire PSG, a long lasting but weak negativity was generally present throughout tracks (see Fig. 3D). Such responses were probably distantly generated as also indicated by the CSD analysis. However, some dispersed examples of unit activation were recorded in layers III and V also in these parts of area 4γ.

Climbing fibre receptive fields of NIA sites

The cutaneous climbing fibre receptive fields were identified by electrical and natural stimulation for all cerebellar nuclear sites investigated. Sites in the forelimb area of NIA were classified into groups and subgroups according to the classification scheme of Garwicz & Ekerot (1994) which was based on the location of the sensitivity centre of the receptive fields. In brief, for sites in group I the sensitivity centre was located distally on the digits, in group II on the dorsum of the paw, in group III on the ventral parts of the paw and forearm and in group IV on the ulnar side of the paw and forearm. Within these main groups, subgroups can be identified on the basis of additional, smaller differences in the distributions of sensitivity centres (Fig. 4). Note that one subgroup of sites that has previously not been distinguished from subgroup IIIb is treated separately here because of its specific cortical projections. It is denoted IIIadist in Fig. 4 and henceforth. These receptive fields differed from those of IIIa sites by being more distal, from those of IIIb sites by being more biased towards the radial side of the paw and from those of Ia sites by including the proximal part of the paw.

Figure 4. Maximal response amplitudes evoked from different types of NIA sites.

Figure 4

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Each bar represents the maximal response amplitude evoked from one site (evoked by a 30 μA double shock or, in a few cases, a 50 μA single shock). Amplitudes are expressed as a percentage of the maximal response evoked in the respective experiment (hatched bars represent maximal response amplitudes of hatched foci in Fig. 7). Sites are arranged in groups and subgroups according to the climbing fibre receptive field classification of Garwicz & Ekerot (1994). A sample receptive field is illustrated for each subgroup. Only sites from 10 experiments in which three or more sites were investigated are displayed. No maximal response amplitude was so close to 0 % that its bar representation was concealed by the 0 % line. rfs, receptive fields.

General aspects of amplitudes and topographical organization of cortical responses evoked from different sites in the cerebellar nuclei

Since there appeared to be differences in response amplitudes between different types of sites, the maximal cortical response amplitudes from different types of sites were compared (Fig. 4). Response amplitudes were normalized to the largest response amplitude within the respective experiments as there were general differences in response amplitudes between experiments (range for IIIb sites: 210-600 μV). The largest responses were evoked from sites in subgroups Ia, IIIa and IIIb. At least one site from one of these subgroups was included in each experiment, a prerequisite for the normalization to give consistent results. In comparison with these subgroups, the maximal response amplitudes of IIIadist sites were distinctly lower despite small differences in receptive fields whereas IIIe/f sites also had large response amplitudes. The weakest responses were invariably found for sites with dorsal or proximal ulnar receptive fields (groups II and IV, respectively). For the distal group I, sites had weaker maximal responses the less radial the receptive field with the exception of the ulnarmost subgroup. Relatively large cortical responses could be evoked from some sites in the hindlimb area of NIA, in particular those with receptive fields concentrated on the medial side of the hindlimb. The cortical responses evoked from sites in the face area of NIA were very weak.

Figure 5 illustrates the topographical distributions in area 4γ of responses evoked by stimulation of different sites in NIA. In Fig. 5A, the topographical distribution of the evoked responses from a IIIb site is illustrated with a few sample recordings and an isopotential map. Nuclear stimulation evoked large surface-positive responses mainly in lateral ASG (Fig. 5AIV). Medially, only weak responses were recorded (Fig. 5AV, AVII and AVIII). Laterally and/or caudally from the projection focus, surface positive responses diminished and were cut short by an increasing negativity with a progressively earlier onset (Fig. 5AI-III). This general pattern of response distribution was the same for most types of NIA sites. Exceptionally among forelimb sites, the IIIa site had an additional, distinct projection focus in the medial PSG close to the caudal border of area 4γ (Fig. 5B II). All isopotential maps were constructed from amplitudes measured at the latency of the maximal surface positivity (at 10.5 ms in Fig. 5A and F; 14 ms in Fig. 5B-E and G). Amplitude measurements were made at many latencies for all sites investigated. In brief, isopotential maps were similar no matter which latency the amplitudes were measured at (cf. Fig. 3A).

Figure 5. Isopotential maps of cortical responses evoked on stimulation of NIA sites.

Figure 5

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In A-G, isopotential maps of cortical responses are shown to the left. Climbing fibre receptive fields of stimulated sites, their classification and location in NIA are shown to the right. Outlines of cortical exposure and of area 4γ are shown with semithick lines. Sample distributions of recording points are indicated by circles in A. Roman numerals in A and B refer to recording points, indicated by stars, from which sample recordings were taken. Same calibrations for all recordings. The data of the following maps were obtained in the same experiments: A and F, B and C, and D and E.

Relationship between the topographical organization of cortical projections and the climbing fibre receptive field of sites

Figure 5 also illustrates the differences in the topographical distribution of responses evoked from the major types of NIA sites. In addition to the profound differences in response amplitudes, large differences in response topographies between sites with ventral and dorsal receptive fields (Fig. 5A and E) and between sites with proximal radial and proximal ulnar receptive fields (Fig. 5B and D) can be seen. The response distribution of sites with distal receptive fields (Fig. 5C) extended far laterally in area 4γ in addition to a partial overlap with those of sites with ventral and proximal radial receptive fields. Quite different topographies were found for the responses evoked from hindlimb and face sites of NIA (see Fig. 5F and G and below).

Overall, we found that response topographies of single sites were more or less unchanged with different stimulation intensities. Different stimulus intensities were tested for a majority of the sites with 30 μA double shock and 50 μA single shock stimulation, for 16 sites in three experiments with 30 and 50 μA single shock stimulation and for 9 sites in two experiments with 50 and 100 μA single shock stimulation. Although not shown, nearly all response topographies were thus observed for at least two different stimulation intensities.

Figure 6 allows a more extensive examination of differences in response topographies between different types of forelimb sites as well as an evaluation of the similarity across experiments between isopotential maps for the same types of site. For example, the first column displays the isopotential maps of three Ia sites in two experiments. Their projection foci (90 %) were found to be very similar in all cases and general similarities in the distribution of isopotential lines at lower amplitudes (30 and 70 %) can also be seen between these three sites (see also isopotential map at 10.5 ms for the Ia site illustrated in Fig. 3A). In contrast, the isopotential maps of the two Ic sites look quite different from those of the Ia sites but similar to each other. More profoundly different isopotential maps were found for group II sites but within this group similarities in isopotential maps between different sites were less pronounced (see also Fig. 7). The consistent distinction of mainly the 90 % levels in the isopotential maps of IIIadist, IIIb and Ia sites (see also Fig. 7) was remarkable considering the relatively small differences in receptive fields and the distinction was further substantiated by the marked difference in maximal response amplitudes (see Fig. 4). Isopotential maps of IIIe/f sites differed from those of IIIb sites by their being biased towards more lateral and rostral parts of area 4γ. In contrast, isopotential maps of group IV sites were consistently focussed to more medial parts of area 4γ.

Figure 6. Comparison of isopotential maps of cortical responses evoked from forelimb sites in NIA.

Figure 6

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Cortical projections from different NIA sites are represented by isopotential lines drawn at 30, 70 and 90 % of their maximal evoked responses (the 30 % level is left out for one site since its low voltage was too close to baseline noise). Outline represents border of area 4γ and the cruciate sulcus. Column alignment indicates group or subgroup identity of stimulated sites according to heading. Symbols at the top left of each map denote sites from same experiments. Maximal response amplitudes are also given at the top. Beneath maps, nuclear locations of sites are indicated (see key in Fig. 1C). Open isopotential lines rostrally indicate extent outside the exposed cortical area. Crosses corresponding to the Ia focus are given for reference.

Figure 7. Foci of cortical responses evoked from NIA sites.

Figure 7

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Display as in Fig. 6 for all sites investigated. For legibility, isopotential lines are only drawn at 90 % of maximal response amplitudes (projection foci). Projection foci of sites with the same type of climbing fibre receptive field are superimposed. Shading indicates multiple foci in isopotential maps of single sites. Hatched foci were considered clearly different from other foci within the respective map and the corresponding nuclear sites are indicated by filled squares.

Figure 7 presents a survey of distributions of cortical projection foci and nuclear locations for all NIA sites. For individual subgroups, these projection foci were generally reproducible between experiments (see Ia sites) which was also true for lower isopotential levels. A few types of forelimb sites, not accounted for in Figs 5 and 6, deserve mention. Ib sites had isopotential maps that were very similar to those of Ia sites although their cortical response amplitudes were consistently smaller (see Fig. 4). The two Id sites had isopotential maps that neither resembled each other nor those of other sites. The isopotential maps of two of the Ie sites were indistinguishable from those of Ia sites whereas the projection focus of one Ie site resembled those of Ic sites, although the distribution of lower isopotential levels differed. The relative similarities in distribution of projection foci between the three IVb sites as compared with the single IVa site may also be noted. Figure 7 further shows that sites within single subgroups were located in a narrow but rostrocaudally extending representation in NIA (in agreement with Garwicz & Ekerot, 1994). Hence the topography of evoked cortical responses varied with the subgroup identity of the stimulated site rather than its nuclear location. Note, however, the single Ia, Ic and Ie sites with ‘atypical’ cortical projection foci (hatched foci in Fig. 7) had nuclear localizations that differed from the remainder of the sites within the respective subgroup (the maximal response amplitudes evoked from these sites were also ‘atypical’, see hatched bars in Fig. 4).

To provide further topographical comparisons for the projections from forelimb sites in NIA, cortical responses evoked from some hindlimb and face sites were also analysed. These sites were found within the hindlimb and face areas of NIA as described by Gibson et al. (1987). All hindlimb sites had projections to lateral ASG, a region of the motor cortex that has traditionally been considered a forelimb motor output region (Fig. 7). Most hindlimb sites had additional projection peaks far rostrally and medially in area 4γ, in the adjacent part of area 6aβ and/or in the medial part of ASG, peaks which distinguished them from the forelimb sites. Some of these peaks are not displayed in Fig. 7 since their amplitudes did not reach 90 % of the maximal responses of the respective sites. Sites with climbing fibre receptive fields on the medial side of the hindlimb had projection foci that were different from those of other hindlimb sites and located mainly caudomedially to the projection foci of forelimb sites (Fig. 7). Note that the responses recorded adjacently to the cruciate sulcus in the medial ASG might be distant reflections of more powerful responses in the main motor representation of the hindlimb, which is buried in the cruciate sulcus (see Nieoullon & Rispal-Padel, 1976). The two sites in the face region of NIA had very weak cortical responses with a common focus medially in PSG (Fig. 7), close to the PSG focus of the IIIa site (Fig. 5B). Both sites had additional, even weaker, projection foci in other regions as well (see Fig. 5G).

In addition, the cortical projections of four NIP sites and three NL sites were also investigated. The overall projection topographies of such sites were quite different from those of NIA sites although the peak responses were still preferentially located rostral to the cruciate sulcus. In agreement with previous reports (Rispal-Padel & Latreille, 1974; Shinoda et al. 1985), NIP sites had projection foci lateral to those of NIA sites whereas NL sites had projection foci medial to those of NIA sites (i.e. in area 6aβ and in medial area 4γ). Overall, NIP sites had weaker cortical projections than NIA sites (corresponding to 30-60 % in Fig. 4) whereas large variations in maximal response amplitudes relative to the maximal response of the experiment were found for NL sites.

Topographical and temporal organization of peripherally evoked potentials in motor cortex

To investigate the relationship between the overall cortical projection area of NIA output and the cortical projection areas of the forelimb skin, a similar analysis to the above was performed for the cortical responses evoked on electrical stimulation of the peripheral sites described in Methods. Isopotential maps of cortical responses for each millisecond after the stimulation (cf. Fig. 3A) revealed that, in contrast to the cortical responses evoked from NIA sites, peripherally evoked responses had several spatially distinct peaks that developed at different latencies. Figure 8A summarizes the findings by illustrating isopotential maps of response amplitudes at a few different latencies for four different stimulation sites on the left forelimb. The illustrated latencies were those that provided the best spatial differentiation of the different peaks.

For each of the four stimulation sites there was a wave of activation that over time spread from the caudolateral part of area 4γ towards its rostral and more medial parts. However, the earliest responses recorded within the cortical exposure were found in area 3b where characteristic potentials were evoked (recording point indicated by triangle in Fig. 8). Different stimulation sites activated distinct subregions of this cytoarchitectonic area. The earliest peaks in area 4γ appeared to represent spread from the adjacently activated regions of area 3b. The onset latencies of these responses were similar to those in area 3b but their peaks had longer latencies. Possibly related to the limited cortical exposure, this type of early response in area 4γ was never seen for the distal radial stimulation site. The second peaks in area 4γ appeared far rostrally and at this latency there was also a distinct peak for the distal radial stimulation site (although consistently at a slightly longer latency than for other stimulation sites). Thus, a small subregion of area 4γ was activated in sequence from lateral to medial from the distal ulnar, radial and ventral stimulation sites. At a third latency, two spatially separate group of peaks occurred medially to the peaks of the second latency. The rostral peaks coincided topographically for the distal stimulation sites whereas input from the ulnar forearm (uln.prox) and face were found progressively more medially. At the same latency, another detailed somatotopic organization appeared caudally where the activation sequence from lateral to medial was from proximal ulnar, distal ulnar, ventral and distal radial stimulation sites. Peripheral input to the region where a IIIb site in NIA projected heavily (see square in Fig. 8) was weak, and projection foci of the two input sources were largely non-overlapping as judged from the surface recordings. However, at least distal peripheral stimulation sites activated units in microelectrode tracks in the lateral part of the IIIb focus. Only weak cortical responses with a temporally stable distribution were found from the face and hindlimb. These responses had, respectively, earlier and later onsets than forelimb responses (Fig. 8A).

Allowing for systematic shifts of some milliseconds in latency between different experiments, the analysis of spatiotemporal peaks revealed a detailed topographical organization that was nearly identical between animals. However, the analysis was performed in deeply anaesthetized animals and slight differences in anaesthesia disrupted the detailed organization seen. In particular, the relative amplitudes of the late peaks close to the cruciate sulcus and at the rostral end of area 4γ were highly variable between experiments, which often resulted in the somatotopic organization of the late caudal peaks described above being less clear.

DISCUSSION

This is the first study in which the organization of cerebellar projections to the motor cortex was investigated for functionally identified sites in the cerebellar nuclei. In addition, the current intensities used for stimulation of these sites were much lower than in previous, related studies (Rispal-Padel & Latreille, 1974; Shinoda et al. 1985). Taken together, the present study provided a previously unprecedented resolution for a systematic analysis of the topographical relationship between the cerebellar nuclei and the motor cortex. An important finding was the relationship between the cutaneous climbing fibre receptive fields of NIA sites and the strength and topographical distribution of evoked cortical responses.

Neuronal elements activated by electrical stimulation in the cerebellar nuclei

A crucial issue for the interpretation of the present results is to what degree the microstimulation activated local nuclear cells in NIA as compared with non-local nuclear cells and locally passing fibres. Unfortunately, the scanty literature on the subject gives virtually no help. Hence, for 30 μA, estimations of the radial spread for neuronal activation vary between 100 and 600 μm (Ranck, 1975). However, from Fig. 2 it appears that spread of stimulating effects to distant neuronal elements was not a major problem in this study and neither did it appear to be a major problem in a recent study of the movements evoked from these sites via the rubrospinal tract (Ekerot et al. 1995; see account below). Note, though, that some activation of distant neuronal elements cannot be excluded since these effects should be relatively weak and thus overshadowed by the responses produced by powerful activation of local nuclear cells.

In order to reach brachium conjunctivum, efferent fibres of NIA should pass mainly ventrally and rostrally, which also appears to be the case in retrogradely labelled cells (McCrea et al. 1978). Hence, the ventralmost stimulation site in Fig. 2 must have been located in the midst of efferent fibres originating from all sorts of NIA sites and possibly other nuclei. The virtually complete absence of cortical responses to such stimulation suggest that the stimulation parameters used here produce poor activation of fibres. A relatively small response was evoked from the site 200 μm ventral to NIA. This response might be explained by stimulus spread into cells inside the nucleus (the upper part of the electrode with an exposed length of 150 μm might actually have been extending into the nucleus) or activation of the dispersed cells commonly seen outside the histologically definable borders of NIA. The idea of relatively poor activation of passing fibres is given support by considering the distribution of cortical responses evoked from different sites together with the relatively well-known topographical organization within NIA of such sites (Garwicz & Ekerot, 1994; and present study). For example, Ic sites should be traversed by fibres from sites in groups II and IV, and IIIb sites should be traversed by fibres from IIIe/f and IVa/b sites but in neither case did the projection foci overlap to a major extent (Figs 6 and 7). Also, the increase in response size with long as compared with short pulse widths (Fig. 1F) is a further suggestion that cells were preferentially activated over fibres (cf. Asanuma et al. 1976). It may appear that the projection from hindlimb sites to the forelimb area of the motor cortex is a clear indication that fibres passing from forelimb sites were activated. However, for hindlimb sites with medial receptive fields, similar projections were found whether they were located adjacently to the forelimb representation or further rostrodorsally in NIA (see Fig. 5F). Due to the topography and fibre orientation in NIA, the latter location is highly unlikely to be traversed by fibres from any forelimb site. Importantly, the particular region receiving the overall most powerful projections from hindlimb sites nearly completely overlapped the region that contains a large number of neurons with axon branches to both cervical and lumbar enlargements (Armand, 1978; see also Shinoda et al. 1976), a region which may thus be less purely related to the forelimb than traditionally assumed.

Apparently high threshold for activation of passing fibres was also found in a recent study of movements evoked via the rubrospinal tract by microstimulation of identified NIA sites (Ekerot et al. 1995). Fibres of group II sites should pass through group III sites but wrist movements of opposite directions were virtually always evoked from the two respective groups of sites. Similarly, elbow extension was only evoked from IIIa sites whereas elbow flexion was routinely evoked from both group IV and other group III sites that are located respectively dorsal and ventral to the IIIa representation in NIA. The seemingly low probability of activating passing fibres in Ekerot et al. (1995) and the present study may be related to the relatively large exposed tips of the microelectrodes. The low current density thus produced may be less effective in activating fibres as compared with neurons.

While the most powerful cortical projections of individual NIA sites were thus probably mainly produced by activation of local nuclear cells, the question of which elements contribute to the less powerful activation surrounding projection foci remains open. Clearly, the highly divergent nature of the neurons in the cerebello-thalamocortical pathway (see below) contributed to the widespread distribution of such low amplitude responses but it is impossible to exclude a contribution from activation of passing fibres and/or distant nuclear cells.

Generation of responses recorded at the cortical surface

Deep pentobarbitone anaesthesia was a prerequisite for obtaining sufficiently stable responses to allow the present topographical analysis but did at the same time depress the thalamocortical excitability. The depression seemingly affected the cerebello-thalamocortical pathways for all sites similarly, as relative differences in maximal response amplitudes were preserved between experiments (Fig. 4).

The basic reversal properties of the cerebellar-evoked cortical responses were similar to those of Sasaki et al. (1973), but the present study provided a more detailed analysis of such responses. The initial component of cerebellar-evoked responses (Fig. 1H), which had its maximal negativity in the deep part of layer III (Fig. 3D), probably corresponded to EPSPs elicited by thalamocortical afferents. Apparently, the major part of the recorded responses consisted of an excitatory process elicited by the thalamocortical EPSP. The linear relationship between the positive and negative peaks with changing response amplitudes and the occasional all-or-nothing disappearance of all but the initial component of the response (Fig. 1G and H) make it unlikely that the excitatory process was due to sequential synaptic activation. Regenerative dendritic activity, which is a salient feature of neurons in layers III and V and easily evoked on stimulation of the ventrolateral thalamic nucleus (VL) (see Castro-Alamancos & Connors, 1996), appears to be a more plausible explanation. The late superficial negative potentials must reflect that the superficial neuronal elements for some reason ceased to act as a source for the layer III sink. This could be explained by assuming that the regenerative activity gradually engaged more superficial dendrites during the time course of the response.

The saturation phenomenon illustrated in Fig. 1D, which resembles the saturation of the thalamocortical volley described by Rispal-Padel et al. (1987), may indicate that the main effect of the microstimulation occurs in local nuclear cells and that the phenomenon is due to saturation of their electrical excitability. However, the gradually decreased latency to peak of the cortical response with stimulation intensities increased beyond saturation level rather suggests that the regenerative activity occurred at shorter latencies in superficial dendrites. This could be explained either by activation of a larger number of thalamocortical afferents or by an increased thalamocortical discharge synchronicity.

Topographical organization of projections to the motor cortex from NIA sites

Most NIA sites projected mainly to lateral ASG. The cortical responses of single sites were distributed over relatively large areas but despite the resulting extensive overlap, projections differed by their relative activation of different parts of lateral ASG (Figs 5 and 6) and by the location of their foci (Fig. 7). The evoked cortical responses presumably reflect activation of a large number of the widely arborizing thalamocortical fibres that are characteristic for VL neurons (Asanuma et al. 1974). Hence peaks of cortical activation should correspond to regions at which the largest number of activated thalamocortical afferents converged. The activation of a large number of thalamocortical neurons was to be expected since a stimulation protocol similar to ours activated wide areas of VL (Rispal-Padel et al. 1987), presumably reflecting divergence in the thalamic projection of nuclear cells. Note, though, that the depth recordings indicated a more focalized cortical activation than suggested by the isopotential maps of the surface responses (see Fig. 3).

Differences in response amplitudes between the different subgroups of nuclear sites probably reflected true differences in cortical projection strength since no difference in average thresholds for movements evoked from different NIA sites through the rubrospinal tract was found (C.-F. Ekerot, H. Jörntell & M. Garwicz, unpublished observations). Sites with distal, radial or ventral receptive fields thus seem to use the output pathway via motor cortex more extensively than sites with dorsal and proximal ulnar receptive fields (Fig. 4). In addition to the relationship between specific types of NIA sites and their maximal response amplitudes, there was also a specific relationship between the climbing fibre receptive fields of sites and the topographical distribution of their cortical projections. Large projectional differences were found between sites with large differences in receptive fields, i.e. between forelimb, hindlimb and face sites (Fig. 5) and among forelimb sites between Ia, Ic, IIIe/f and group IV sites (Figs 6 and 7). Smaller differences in receptive fields between sites were accompanied by smaller differences in cortical projections (see Ia, Ib, IIIadist and IIIb sites, Figs 6 and 7, and also IVb and IVa sites in Fig. 7). Garwicz & Ekerot (1994) found a general relationship between the degree of similarity in receptive fields and topographical nearness of NIA sites. The present results suggest that this relationship can be extended to include the degree of similarity in motor control as well.

The spatiotemporal organization of peripheral input to motor cortex

Although other authors have previously noted regional differences in latencies of peripherally evoked responses within the motor cortex (see Morse & Towe, 1964; Andersson, 1986), the present study was made at a higher resolution and/or with a more complete coverage of area 4γ than in previous investigations. By using a temporally rigid analysis of potentials evoked by needle electrodes in the forelimb skin, several spatially discrete response foci with different latencies were seen for each area of the skin. Since the corresponding temporal peaks for different skin areas were located in adjacent cortical regions several somatotopic maps were seen.

The rapid changes in topographical distribution of peripheral input were in marked contrast to the temporally stable distribution of cerebellar projections (see Figs 3A and 8) and probably indicate that there exist several different routes for the peripheral input to the motor cortex. Indeed, the data of Oscarsson & Rosén (1966) suggest that the spinocervical pathway could be responsible for some of our medial pericruciate responses whereas the dorsal funiculus pathway could be responsible for responses evoked in the lateral part of area 4γ. In addition to different pathways, different cortico-cortical connections may also be involved. It has been shown that the late peaks at the tip of the cruciate sulcus (as described in the present study) are partly abolished by lesions of cortical regions lateral to the coronal sulcus, while cortical responses evoked from brachium conjunctivum are largely unaffected (Andersson, 1995). The small rostral region to which input from all three distal skin sites converged appears to be the only part of precruciate area 4γ that receives input from the parts of areas 1 and 2 that are located just rostral to the ansate sulcus (Yumiya & Ghez, 1984). However, after removing the region that received the earliest input in the present study, Morse & Towe (1964) did not find any effect on pericruciate responses.

Projections to the motor cortex from NIA sites and forelimb skin

Although NIA sites were, via the climbing fibres, partly activated from the same skin areas that were electrically stimulated to study the peripheral input to the motor cortex, the cortical responses of these two input sources had mainly different distributions (Fig. 9). In addition, input from the skin reached different regions of the motor cortex (approximately caudal, lateral, medial and rostromedial lateral sigmoid gyrus (LSG), respectively, see Fig. 9) through different pathways. These gross topographical differences in cortical activation presumably reflect gross differences in motor control function (cf. Introduction), but it is unclear at the present stage what these motor control functions would be (cf. Lemon, 1988).

Figure 9. Distribution of cortical responses evoked from forelimb sites in NIA and from peripheral skin sites.

Figure 9

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Thick black lines indicate projection foci for all forelimb sites of NIA (see Fig. 7). Hatched areas correspond to the spatiotemporal peaks of skin sites on the forelimb and face as illustrated in Fig. 8. To reveal the double peaks at the longest latencies, projection foci of the peripheral input were drawn at 80 % of the maximal response amplitude at each latency.

Concluding remarks

The present study used the previously delineated organization in the forelimb area of NIA as a frame of reference to demonstrate the existence of a detailed and relatively constant topographical organization in a structure where the contrary has been emphasized in some recent studies (see Nudo et al. 1996). Although temporally more complex, the topographical organization of the peripheral input to the motor cortex was also found to be very similar between animals. The cerebellar and peripherally evoked responses had largely non-overlapping foci and the two afferent sources in combination provide a relatively constant topographical frame of reference for a major part of the motor cortex. Such frames of reference are important to relate to for studies aimed at understanding the functional organization of the motor cortex.

Acknowledgments

This work was supported by funds from the Swedish Medical Research Council (project no. 8291), the Medical Faculty of the University of Lund, the Royal Physiographic Society in Lund, Magn. Bergvalls Stiftelse, Dr P. Håkanssons Stiftelse, Greta and Johan Kocks Stiftelser, Thorsten and Elsa Segerfalks Stiftelse and Crafoordska Stiftelsen.

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