Comparison of response properties of dorsal and ventral spinocerebellar tract neurons to a physiological stimulus

Brain Research, 369 (1986) 125-135 Elsevier

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Comparison of Response Properties of Dorsal and Ventral Spinocerebellar Tract Neurons to a Physiological Stimulus J.H. KIM1, T.J. EBNER 1,2and J.R. BLOEDEL3

Departments of lNeurosurgery and 2Physiology, Universityof Minnesota, Minneapolis, MN55455 and 3Divisionof Neurobiology, Barrow Neurological Institute, Phoenix, AZ 85013 (U.S.A.) (Accepted July 30th, 1985)

Key words: dorsal spinocerebellar tract-- ventral spinocerebellar tract-- spinal cord-- cerebellum - - cutaneous input

The response characteristics of dorsal spinocerebellar tract (DSCT) neurons and ventral spinocerebellar tract (VSCT) neurons to the cutaneous inputs applied to footpads were studied in the cat. Three different wave forms were used: (1) step displacement of varying amplitudes (0.01-3.5 ram); (2) constant amplitude ramps with different slopes (5-120 ram/s); and (3) constant amplitude sinusoidal displacements of varying frequencies (1-20 Hz). Both DSCT and VSCT neurons responded phasically to cutaneous stimuli of different wave forms. The phasic responses were related to both the amplitude and velocity of the peripheral stimulus. However, the responses of DSCT neurons were graded over only a very narrow, low range of stimulus intensities, whereas the responses of VSCT neurons were graded over a larger range of skin indentation up to 3 mm. Only the DSCT neurons exhibited some length sensitivity to ramp stimuli, and only DSCT neurons were activated repetitively by periodic stimuli. These results suggest both DSCT and VSCT can transmit exteroceptive information but respond selectively to different features of these stimuli.

INTRODUCTION The dorsal spinocerebellar tract (DSCT) and the ventral spinocerebellar tract (VSCT) are the two major direct mossy fiber afferent systems projecting to the cerebellar cortex from the lumbar spinal cord. These two systems differ in their cells of origin, spinal pathways, and sites of termination in the cerebellum 7,12,33,35,42. This paper focuses on a comparison of the responses of these two afferent systems to the same natural cutaneous stimulus. The D S C T originates from the nucleus dorsalis (Clarke's column) in the thoracic and upper lumbar segments of the spinal cord, projects through the dorsolateral funiculus and inferior cerebellar peduncle, and terminates in the vermal and paravermal regions of the ipsilateral cerebellar cortex 7,31,32,39. The organization of the VSCT projection is quite different. This pathway originates principally from neurons located in the lateral region of the ventral horn at L 3 - L 6 . These cells cross the midline near their level

of origin, ascend contralaterally through the ventrolateral fasciculus, and enter the cerebellum through the superior peduncleT,30, 32. Within the cerebellum the majority recross to the ipsilateral side and terminate in the paravermal region of the anterior lobe. The fibers which do not recross terminate in the same lobules of the cortex contralateral to the cell bodies of their origin. Both afferent systems are responsive to cutaneous inputs. Based on extracellularly recorded responses of DSCT cells, cutaneous inputs are believed to project principally to a separate population, the exteroceptive subdivision33-35, 4z. These neurons are responsive to at least 3 classes of cutaneous afferents: (1) slowly adapting receptors located in the footpads; (2) phasic and tonic mechanoreceptors located on the hairy skin; and (3) flexor reflex afferents 34. In addition to receiving some polysynaptic inputs, the dendrites of single D S C T neurons receive as many as 50 synaptic contacts from a single primary afferent47. 48. Cells in the proprioceptive subdivision of the DSCT,

Correspondence: J.H. Kim, University of Minnesota, Department of Neurosurgery, Box 96 Mayo, 420 Delaware Street S.E., Minneapolis, MN 55455, U.S.A. 0006-8993/86/$03.50 © 1986 Elsevier Science Publishers B.V. (Biomedical Division)

126 although predominantly responsive to proprioceptive inputs, are also activated polysynaptically by cutaneous afferents z2-24. A single VSCT neuron usually receives both cutaneous and proprioceptive afferent input 38,44. Cutaneous inputs to the VSCT are mediated principally by polysynaptic pathways which are organized consistent with the comparator hypothesis of Lundberg32. According to current views, the DSCT and the VSCT convey different information to the cerebellum. The DSCT is felt to convey information concerning peripheral exteroceptive and proprioceptive inputs 3.33,35,42. The VSCT is felt to be principally responsive to the modulation of descending pathways involved in the initiation and performance of movements2, 3.32. In support of this hypothesis, severing the dorsal roots in a locomoting cat depressed the modulation of DSCT neurons while the modulation of VSCT neurons was unimpaired2, 3. In contrast to this view, initial studies in our laboratory indicated that both the DSCT and VSCT neurons are well modulated by exteroceptive stimuli 25. At present there are no data comparing the responses of VSCT and DSCT neurons to similar natural peripheral inputs. The present studies were designed to test the hypothesis that DSCT and VSCT neurons are modulated by exteroceptive stimuli but encode different features of the same stimulus. This hypothesis was tested by comparing the response characteristics of VSCT and DSCT neurons with overlapping receptive fields to the same stimulus applied to the same region of the body surface. The stimulus was designed to mimic exteroceptive inputs encountered during footfall. This approach contrasts with previous studies which examined the receptive field characteristics of DSCT and VSCT neurons to punctate stimuli applied to multiple sites on the extremities 34. An abstract of some of this work has been presented 25. MATERIALS AND METHODS

Animal preparation These experiments were performed using 51 adult cats (2.0-4.0 kg) anesthetized with a-chtoralose (60 mg/kg). The right axitlary artery and vein were catheterized to monitor blood pressure and to administer drugs, respectively. A tracheostomy was performed,

bilateral pneumothoraces placed, and each animal was artificially respired. The animals were paralyzed with gallamine triethiodide and expiratory CO2, blood pressure and body temperature were maintained within physiological ranges. A posterior craniectomy was performed to stereotaxically placed stimulating electrodes in the ipsilateral inferior peduncle (P 9.0, H 3.5, L 5.5) or in the contratateral superior peduncle (P 3.0, H 3.0, L 3.0) for antidromic identification of DSCT or VSCT neurons, respectively. DSCT and VSCT neurons were studied in separate animals. The stimulating electrode array consisted of a rake of two concentric bipolar electrodes spaced 1 mm apart as described elsewhere6. 8. Two dorsal laminectomies were performed. A caudal laminectomy at the L1-S1 region exposed the lumbar enlargement to record DSCT or VSCT neuronal activity. A rostral laminectomy near the T 6 - T 7 level permitted placement of a bipolar stimulating electrode on the cord. Following the laminectomies, an oil pool was formed from the skin flap and maintained at 38 + 1 °C by a feedback controlled heating circuit. The criteria used for antidromic activation of VSCT and DSCT cells were: (1) the ability to follow high frequency stimulation (100-300 Hz) with variation in latency not exceeding 0.2 ms; (2) change in latency of less than 0.2 ms when the stimulus intensity was increased from threshold to supramaximal amplitudes; and (3) collision of the antidromic spike with an orthodromic spike evoked by stimulating the receptive field 6. As a further requirement for identification, DSCT neurons were checked for antidromic activation from the rostral cord ipsilateral to the recording site. Similarly, VSCT neurons were required to be activated antidromically from the contratateral side of the rostral cord. After a neuron was positively identified as a DSCT or VSCT unit, the receptive field was carefully determined by applying different natural stimuli to the receptive field of the ipsilateral hindlimb. Only DSCT and VSCT neurons responding to exteroceptive stimuli with receptive fields on the ipsilateral footpads were studied. To apply the stimulus to the ipsilateral footpads the leg was flexed at the knee, and the tibia and dorsum of the foot were secured in molding clay, leaving the footpad exposed. The stimulus probe consisted of a flat, circular surface with a diameter of 30 mm. The

127 stimulus was adjusted so that the entire plantar surface of the footpad was contacted by the probe. Driven by a mechanical vibrator, the position of the probe was monitored using a linear variable differential transducer placed in series between the probe shaft and the vibrator. Special care was taken to maintain a constant relationship between the stimulus surface and the footpads throughout the evaluation of each cell. Three different stimulus waveforms were applied: (1) a step displacement with varying amplitude (0.01-3.5 mm amplitudes, 167 ms duration); (2) a constant amplitude ramp displacement with varying velocity (5-120 mm/s); and (3) a constant amplitude (3.0 mm) sinusoidal displacement with varying frequency (1-20 Hz).

Recording In most cats 2 M NaC1 filled glass microelectrodes (2-3 M ~ ) were used to isolate the neurons. In other animals, glass microelectrodes filled with pontamine sky blue (2-3 MQ) were used to label the recording sites17.31. Neuronal activity evoked by step or ramp displacement was discriminated, and poststimulus time histograms (PSTHs) were constructed on-line. Neuronal responses to sinusoidal stimuli were analyzed by constructing cycle histograms. Separate PSTHs or cycle histograms were averaged over 50 sweeps for each stimulus paradigm. The displacement and discriminated spike activity were recorded on magnetic tape for additional off-line data analysis. To mark the recording site, pontamine sky blue dye was injected with a cathodal 5/~A current for 3 min. At the end of the experiment the position of the cerebellar stimulating electrode was marked by passing current. The animal was then perfused with 10% formalin solution. The spinal cords were sectioned into 60/~m slices and stained with cresyl violet. The recording sites marked by pontamine sky blue were examined, and the site of the cerebellar antidromic stimulating electrode was histologically confirmed. Data analysis Phasic response to step displacement. Both DSCT and VSCT neurons responded to the step displacement with a brief, phasic increase in spike discharge (see Fig. 1A, D). This response component was quantified by first choosing a 40 ms time window based on the examination of the data from all cells.

Within this window, which began at the onset of displacement, the total number of spikes was determined for each step amplitude. The phasic response amplitude was expressed as percentage of the maximal response and plotted against step displacement. Similarly the velocity of each step was determined and the normalized phasic response component plotted against step velocity. Response to ramp displacement. In addition to an initial phasic component VSCT and DSCT neurons usually responded to the ramp displacement with a longer duration monotonic increase in spike discharge rate (see Fig. 1B, E). This longer duration component was quantified in two ways. First, linear regression analysis was used to determine the slope of this non-phasic component. Expressed as the number of spikes per bin per unit time, this slope was plotted against ramp velocity. Secondly, to evaluate the velocity dependence of a neuron's response to the ramp, a time window was set over the last half of the ramp duration, and the average spikes per bin was calculated for this period. This quantity was then plotted against the ramp velocity for each cell. RESULTS

General features of the DSCT and VSCT neurons In 19 cats, 51 DSCT neurons responded to mechanical stimulation of glaborous skin on the footpads and/ or of hairs surrounding the footpad. These DSCT neurons were antidromically activated by stimulation of the ipsilateral inferior peduncle with a mean latency of 4.06 + 2.06 (n = 46) and a range of 2.8-7.2 ms. Most DSCT cells with cutaneous receptive fields were located at cord level L4-L6 at the end of Clarke's columnS0. Neurons responding antidromically to stimuli in the ipsilateral inferior peduncle but located at the L6-$1 level of the cord were also studied. Among the 13 DSCT neurons marked using pontamine sky blue, 8 cells were found in Clarke's column. The remaining were located just caudal or caudolateral to Clarke's column in Rexed's laminae VI and VII. Sixty-two VSCT neurons having cutaneous receptive fields on the footpad were isolated in 32 cats, and their responses to different waveform stimuli were compared with those of DSCT neurons. The latencies of their antidromic activation from the contralat-

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with a mean of 6.1 ___ 1.9 ms (n = 41). All the VSCT cells studied were located at the L6-S1 cord level. Histological examination of 11 cells marked with dye

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Representative responses of a DSCT (Fig. 1 A - C ) and VSCT (Fig. 1 D - F ) neuron to the different stimulus waveforms applied to the footpad are shown in Fig. 1. Following the 3 mm step displacement (upper traces in Fig. 1A, D) both cells responded with a phasic increase in spike discharge with an 8-10 ms latency. Little spike activity was associated with the plateau phase of the displacement. The response latencies measured from the onset of the step displacement (3 mm) were similar for these two groups of neurons. The mean latency was 9.15 + 1.8 ms (n = 42) for the DSCT neurons and 9.32 + 3.3 ms (n = 32) for the VSCT neurons. Generally DSCT neu-

rons responded with a greater number of spikes per stimulus than VSCT neurons (Figs. 1 and 2). Occasionally, for both groups of cells the first phasic response was followed by a second component with a latency of 20-30 ms. In most DSCT neurons the response amplitude was not significantly reduced when the step or ramp displacements were applied at rates above 4 Hz. However, the response amplitude of most VSCT neurons was reduced with stimulus rates above 1 Hz. To minimize this effect, the rate of ramp or step stimuli was always less than 1 H z . In Fig. 1B and E, the responses of the same DSCT and VSCT neurons to identical ramp stimuli (12 mm/s velocity, 3 mm amplitude) applied on the footpad are shown. The DSCT neuron (Fig. 1B) responded with a brief burst of action potentials at a short latency followed by a gradual increase in the firing rate which was associated with the increasing ramp amplitude. In contrast, the VSCT neuron (Fig. 1E) responded at the onset of the ramp stimuli with a small phasic response. More than half of the VSCT neurons failed to respond to ramp stimuli with a velocity lower than 60 mrn/s. Typical of most DSCT neurons, the sinusoidal stimulus (3 mm amplitude, 10 Hz) evoked a large response during the push phase of the cycle (Fig. 1C). In contrast, VSCT neurons were usually unresponsive to sinusoidal stimuli (Fig. 1F).

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Differences in the responses of DSCT and VSCT neurons to graded amplitudes of step stimuli are demonstrated in Fig. 2. As the amplitude of step displacement was gradually increased, the DSCT neuron's response was saturated at a low amplitude (Fig. 2A-C). The VSCT neuron's phasic response increased over a wider range of step amplitudes (Fig. 2D-F). Occasionally a phasic off-response t o the step displacement, as shown in Fig. 2 A - C for the DSCT cell, was observed in both types of neurons. To examine further the dynamic range over which these two populations of cells respond, the relationship of response amplitude to the amplitude and velocity of the step stimulus was determined. Confirmation that DSCT neurons saturate at much lower step amplitudes than VSCT neurons is clearly demonstrated in Fig. 3A and B. Over the same range of step amplitudes, the responses of the majority of the DSCT cells (Fig. 3A) were maximal or near maximal

130 at lower step amplitudes than the responses of VSCT cells (Fig. 3B). Furthermore, there was considerably more variability among the DSCT neurons. A linear regression analysis of the slope of each responseamplitude curve revealed that the slopes for the VSCT neurons (Fig. 3C) fall in a relatively narrow range (mean 37.94 + 14.88, n = 12). However, the slopes of the DSCT response-amplitude curves had greater variation (range 26.67-920.0, n = 14) and a much larger mean (200.8 + 308.9). For 9 DSCT cells (not all are plotted in Fig. 3A) the slopes could not be calculated since they saturated at the lowest amplitude studied. These cells were not included in the mean. For the 4 DSCT neurons responsive to very small amplitudes of step displacement the slopes were 200-300 times larger than the average VSCT slope. However, a few DSCT cells had slopes low enough to fall within the range of the VSCT cells. As anticipated, the slopes for DSCT and VSCT neurons were significantly different (Student's t-test, P < 0.005). Quantification of the step amplitudes at which saturation occurred was carried out by determining the step amplitude required to evoke a response that was 80% of the maximal response. The ampfitude of the phasic component of each cell's response was calculated as described in the Methods using the same time window (40 ms) for both groups of cells. Stimulus saturation amplitudes are plotted in Fig. 4. The majority of DSCT cells (Fig. 4A) were 80% saturated at amplitudes less than 1 mm (mean 0.65 _+ 0.61, n = 38). Notice that many (13 of 38) of these cells were 80% saturated at the smallest stimulus amplitude used systematically in these experiments, 0.225 mm. In contrast most VSCT neurons (Fig. 4B) did not reach 80% maximum response until the step amplitude exceeded 1.0 mm (mean 1.73 _+ 0.60, n = 29). Among the 13 DSCT neurons whose response amplitude was more than 80% of maximum at the step amplitude of 0.225 mm, 5 cells were further tested at step amplitudes ranging from 0.015 to 0.225 mm. As expected the phasic response was finely graded over this range of step amplitudes. These results indicate that most DSCT neurons have a dynamic range over a lower range of stimulus amplitudes and saturate at a lower intensity than VSCT neurons. The phasic component of the responses of the DSCT and VSCT neurons was also plotted against

the velocity of the step displacement (Fig. 5A, B). The remarkable similarity between the responseamplitude curves and the response-velocity curves in both types of cells strongly suggests that the amplitude dependence of the responses may in part be due to the associated increase in stimulus velocity at the higher step amplitudes.

Response to ramp stimuli The responses to ramps of varying velocities but constant amplitudes were studied in 36 DSCT and 35 VSCT neurons. A typical response profile for a DSCT neuron to the ramp is shown in Fig. 6A and B (see also Fig. 1B). Among the 36 DSCT cells, 26 neurons responded to the ramp with an increasing discharge rate over its time course. This type of response was present in some cells in which an initial phasic component was evoked (see Fig. 1B). In 7 cells the later response component consisted of an elevated but constant discharge rate throughout the duration of the ramp. This response characteristic was not altered even when the ramp velocity was increased to 120 mm/s. Only 3 responded with a decreasing slope over the time course of the ramp. The response of 35 VSCT neurons to the ramp stimuli could be categorized into 3 types: (1) a phasic peak at the onset (Fig. 1E) and some increase in activity during the remainder of the ramp (n = 10); (2) a phasic peak followed by a gradual decrease in spike discharge during the rest of the ramp (Fig. 6D, n = 19; or (3) no response up to the maximum ramp velocity of 120 mm/s (n = 6). The responses to the ramp stimulus were quantified by determining the slope of the longer duration, non-phasic component using a linear regression analysis. Position sensitivity would be expected to produce positive slopes which increase with ramp velocity. In Fig. 6 the calculated regression line for the response of a DSCT (Fig. 6B) and a VSCT (Fig. 6D) cell is indicated as a dashed line. When the slope is plotted against ramp velocity, the majority of DSCT cells (n = 15) had increasing slopes with increasing velocity (Fig. 7A). Only one had a decreasing relationship to ramp velocity. There were 7 DSCT neurons with a slope near zero at all velocities (not shown). However, the slopes determined from the responses of 10 VSCT neurons were near zero at the lower ramp velocities and became negative at the

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higher ramp velocities (Fig. 7B). The later component of the response was further analyzed by determining the average number of spikes/bin over the last half of the ramp. Velocity sensitivity would be expected to produce an increasing amplitude with increasing velocity. This average was plotted against ramp velocity for each cell (Fig. 8). A correlation coefficient was calculated for each plot and those with a correlation coefficient greater than 0.9 were further analyzed by a linear regression. The mean slope is 0.085 (S.D. + 0.05, n = 20) for the DSCT neurons and 0.108 (S.D. + 0.096, n = 19) for the VSCT neurons. These values are not significantly different based on the Student's t-test. The similarity in the slopes of the VSCT and D S C T neurons suggests no difference in the velocity sensitivity of these two populations. A

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Response to sinusoidal waveform stimuli A sharp difference was observed in the responses of DSCT and VSCT neurons to sinusoidal stimuli. As shown in Fig. 9 A - D , the discharge of the D S C T cell was extensively modulated by a constant amplitude (3 ram) sinusoidal stimulus over frequencies ranging from i to 20 Hz. All D S C T cells studied responded in this manner. In contrast, 25 of 35 VSCT neurons examined did not respond to the sinusoidal stimulus over the same frequency range at the same amplitude. The amplitudes used were well above threshold for VSCT cells, based on, their responses to the step stimuli. In 10 VSCT neurons modulation of their discharge rate was observed at lower frequencies (1-7.5 Hz), as shown in Fig. 9 E - H . No VSCT neuron was modulated with t h e ' d e g r e e of phase locking commonly observed for D S C T neurons. DISCUSSION This study has examined and compared the re-

132 sponses of VSCT and DSCT neurons to a consistent peripheral stimulus applied to the same region of the body surface. The entire surface of the footpads was contacted by the stimulus to mimic the spatial distribution of exteroceptive stimuli encountered during normal motor behavior. Previous studies of the exteroceptive inputs to these spinocerebellar systems focused on describing their response properties based on an examination of discrete features of each individual cell's receptive field 34. In contrast, the present study examined the responses of a population of DSCT and VSCT neurons to one specific physiological stimulus to gain insights regarding how this stimulus is encoded by spinocerebellar neurons. In evaluating responses of these afferent systems, this approach may be more relevant since the information they transmit is not used for sensory discrimination. The importance of receptive field characteristics in ascending somatosensory pathways to perceived modality and spatial resolution is well documented 1.17.30.37.46.51. In contrast, the spatial distribution of the receptive fields observed for spinocerebellar neurons may be important principally for determining the region of the body surface to which they respond rather than the spatial resolution of the system. Therefore, this study focused on their response properties to stimuli of different velocities, intensities and periodicities requiring only that a portion of the cell's receptive field be within the stimulated area. The data from these experiments demonstrate that DSCT and VSCT neurons respond quite differently to the same exteroceptive stimuli. The response threshold to step displacements was appreciably lower for DSCT neurons than VSCT neurons. The thresholds for DSCT cells were consistently less than 200 ~m and were as small as 15 ~m for some cells. This observation is consistent with previous studies by Eccles et al. 10 that the threshold for the activation of mossy fibers recorded in the cerebellar white matter to skin displacements is as low as 10 ~m. Most DSCT neurons saturated at lower amplitudes of step displacements than VSCT neurons. These observations suggest these two afferent systems operate over a different range of stimulus intensities. Because the saturation intensity for the activation of DSCT neurons was very low (often approximately 100 ~m) the initial response of these cells to phasic

stimuli similar to those encountered during walking movements (i.e. footfall) would likely be saturated. Gradations in the intensity of these stimuli would not likely be encoded by this system. However, VSCT neurons often had graded responses to step stimuli up to 3000 /~m of footpad indentation, an operating range over which it would be possible to encode the intensity of phasic cutaneous stimuli during normal motor activity. Analysis of DSCT and VSCT neurons to step displacements (Figs. 4 and 5) showed that the phasic component of their responses is related to both the amplitude and velocity of the input. Since the velocity of the step increases with increasing step amplitude, it is not possible to separate velocity and displacement sensitivities based only on this stimulus. However, in the analysis of velocity sensitivity using ramp stimuli, there was a considerable difference in the relationship of ramp velocity and response amplitude between these two populations of neurons. As argued above, neurons with considerable length sensitivity would display a proportional relationship between the slope of the later response component and ramp velocity (Fig. 7). At lower ramp velocities this relationship was generally absent, many DSCT and VSCT neurons having slopes of zero over the lower range of velocities. However, at velocities above 30 ram/s, the longer duration component of the responses of the DSCT cells showed a proportional relationship while the responses of most VSCT neurons did not, indicating that DSCT neurons possess a greater length sensitivity. Interestingly both VSCT and DSCT cells displayed some velocity sensitivity, and based on the average slopes of the plots in Fig. 8A and B, the sensitivities were similar. An important characteristic of the action potentials generated by DSCT neurons is the afterhyperpolarizationU.13-15,20,22. 23 which would be expected to play a significant role in determining their discharge pattern in response to peripheral stimuli. The absence of a tonic response to the step stimuli may be partially based on this property. Following the phasic increase in spike discharge at step onset, the cell's excitability may be sufficiently reduced to prevent discharge throughout the plateau phase, at least for the plateau durations in this study. The ramp stimulus failed to evoke an initial phasic component in many cells (Fig. 6A, B). This may have enabled the gradual

133 increase in cell discharge during the ramp observed for many DSCT neurons. Also, some of the non-linear discharge characteristics during the ramp may reflect this afterhyperpolarization. A strictly proportional linear increase in discharge rate of the DSCT neurons relative to the velocity of the ramp stimulus would be very unlikely for the short duration ramps used. However, the duration of the afterhyperpolarization 13-~5 makes it unlikely that this mechanism completely accounts for the lack of a tonic response to maintained stimuli. Presumably additional mechanisms are involved. Some characteristics of the DSCT responses to ramp stimuli are similar to tho~e of primary muscle spindle afferents 18. Both primary afferents and DSCT neurons typically respond to ramp stimuli with an initial phasic component followed by a second component with a time course reflecting that of the ramp stimulus. However, in these experiments the peripheral stimuli activate principally exteroceptive inputs. Based on the response characteristics of cutaneous footpad receptors 34, one interpretation is that the phasic responses of DSCT cells may reflect input from rapidly adapting receptors while the longer duration components reflect input from slowly adapting receptors. However, DSCT neurons did not show a tonic response component to a step displacement. This observation might suggest that slowly adapting receptors are not contributing significantly to the DSCT. The longer duration responses encoun.tered during ramp stimuli may reflect the progressive spatial recruitment of receptors as the ramp amplitude increased. Based on this supposition, rapidly adaptingcutaneous receptors may provide the dominant input to DSCT cells. The difference between the responses of VSCT and DSCT neurons to ramp stimuli may be partly related to the differences in the spinal organization of synaptic inputs to these two populations of cells. Exteroceptive stimuli activate polysynaptic pathways to DSCT neurons26. 29, and polysynaptic reflex inputs to VSCT neurons have been widely documented7,18.19. Based on the circuitry serving as the basis for the comparator hypothesis of Lundberg32, the activation of peripheral cutaneous inputs would be expected to activate a combination of excitatory and inhibitory reflex pathways to VSCT cells. This complexity would very likely affect the responses to longer dura-

tion stimuli such as the ramps used. Conceivably the action of these inhibitory reflex inputs could be responsible for the consistent reduction of the responses over the time course of the ramp stimuli (Fig. 5). The complexity of excitatory and inhibitory segmental inputs to VSCT cells may, also be partly responsible for the striking differences in responsiveness observed for periodic inputs such as sinusoidal stimuli. Although DSCT neurons were well modulated by periodic exteroceptive stimuli, VSCT neurons were generally poorly responsive. Interestingly, many VSCT neurons were unresponsive to low frequency stimuli implying that these neurons would not be activated repetitively during normal locomotion. Although DSCT neurons would be responsive to successive and repeated stimuli encountered during cyclic motor behavior, VSCT neurons would only respond to intermittent stimuli or perturbations during normal locomotor activity. To summarize, both VSCT and DSCT neurons respond phasically to cutaneous stimuli of different waveforms. These phasic responses have a relationship to both the amplitude and velocity of the peripheral stimulus. However, the responses of DSCT neurons are graded over a very narrow, low range of stimulus intensities, whereas the responses of VSCT neurons can be graded over a range of skin indentations up to 3.5 mm. Only DSCT neurons are capable of responding somewhat proportionally to ramp stimuli of different velocities. Lastly, only DSCT neurons can be activated repetitively by periodic stimuli applied to the footpad. Based on these similarities and differences in the response properties of DSCT and VSCT neurons, it is hypothesized that the DSCT provides information to the cerebellum regarding details of motor behavior throughout their time course, even when the behavior is predictable and/or repetitive. Low intensity, phasic stimuli would be faithfully transmitted by the DSCT but not the VSCT. The responses to step displacements suggest the intensity of larger amplitude phasic stimuli may not be conveyed via the DSCT. This hypothesis is also consistent with the proposal by Houk et al. regarding signals evoked in the central nervous system by proprioceptive afferent fibers 21. Because these proprioceptive afferents have only a low power relationship to velocity or any

134 other p r o p e r t y of the peripheral stimulus, they proposed that these afferents signal 'events' such as the changes in muscle stretch or the changes in the gamma m o t o n e u r o n activation. However, the response characteristics of the D S C T indicate it need not be limited to signaling only the occurrence of events. Information concerning the velocity and displacement components of the stimuli can be conveyed by this pathway. Afferent information associated with the locomotor step cycle could be adequately processed by the DSCT. Because the D S C T is comprised of an exteroceptive and proprioceptive subdivision, it is well suited for conveying information regarding both cutaneous and proprioceptive inputs. Previous hypotheses regarding the function of the VSCT emphasized the importance of inputs from descending pathways. The present observations indicate that peripheral cutaneous inputs may have a greater effect on the excitability of VSCT neurons than previously appreciated. The data indicate that the VSCT is capable of signaling the occurrence and the magnitude of phasic cutaneous stimuli over an amplitude range c o m p a r a b l e to that for stimuli encountered during m o t o r behavior. A l t h o u g h poorly

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