Signalling of static and dynamic features of muscle spindle input by external cuneate neurones in the cat

Abstract

1. The present experiments examined the capacity of external cuneate nucleus (ECN) neurones in the anaesthetized cat to respond to static and vibrotactile stretch of forearm extensor muscles. The aim was to compare their signalling capacities with the known properties of main cuneate neurones in order to determine whether there is differential processing of muscle spindle inputs at these parallel relay sites. 2. Static stretch (<= 2 mm in amplitude) and sinusoidal vibration were applied longitudinally to individual muscle tendons and responses recorded from single ECN neurones. The muscle-related ECN neurones that were sampled displayed a high sensitivity to both static and dynamic components of stretch, including muscle vibration at frequencies of 50-800 Hz, consistent with their dominant input being derived from primary spindle afferent fibres. 3. In response to ramp-and-hold muscle stretch, ECN neurones resembled their main cuneate counterparts in the pattern of their responses and in quantitative response measures. Their coefficients of variation in interspike intervals during steady stretch ranged from approximately 0.3 to 0.7, as they do in main cuneate responses, and their stimulus-response relations were graded as a function of stretch magnitude with low variability in responses at a fixed stretch amplitude. 4. In response to muscle vibration, ECN activity was tightly phase locked to the vibration waveform, in particular at frequencies of <= 150 Hz, where vector strength measures (R) were high (R >= 0.8) before declining as a function of frequency, with R values of approximately 0.6 at 300 Hz and <= 0.4 at 800 Hz. Both the qualitative and quantitative aspects of ECN responsiveness to the vibro-stretch disturbances were indistinguishable from those of the main cuneate neurones. 5. The results demonstrate a high transmission fidelity for muscle signals across the ECN and no evidence for differential synaptic transmission across the parallel main and external cuneate nuclei. Earlier limitations observed in the capacity of cerebellar Purkinje cells to respond to primary spindle inputs must therefore be imposed at synapses within the cerebellum.

Figure 3. Effect of muscle vibration frequency on phase locking of ECN neurone responses to muscle vibration

A-C, phase-scatter plots and cycle histograms constructed from the responses of an ECN neurone to 5 applications of 1 s trains of vibration (20 μm amplitude) applied at frequencies of 150, 300 and 500 Hz, respectively. Phase-scatter plots show the time of impulse occurrences (single dots) during each cycle period (ordinate) as a function of time after the onset of the 1 s vibration train (abscissa). Cycle histograms share the same ordinate as scatter plots and display the cumulative distribution of impulses within the vibration stimulus cycle (abscissa: number of impulses in each of the 50 bins into which each ordinate scale is divided). R (resultant) value accompanying each distribution shows the level of phase locking in response (see text). D, tightness of phase locking indicated by R (resultant) values, plotted as a function of amplitude for vibration frequencies in the range 50-800 Hz (for the same neurone whose data are presented in A-C). E, representative points of the same data shown in D, re-plotted to show phase locking as a function of frequency. The 0 Hz value at the origin of the abscissa represents values of R obtained in the absence of vibration.

Figure 1. Responses of ECN neurones to static muscle stretch

A, 2 mm ramp-and-hold stretch (0.5 s onset and offset ramps; waveform at top) applied to the IPr muscle generated a maintained response in an ECN neurone, shown by the impulse record (top trace), the peristimulus time histogram (constructed from 6 successive responses; bin width 80 ms) (middle), and the instantaneous frequency plot (bottom). B, stimulus-response relations for 7 ECN neurones tested over the 2 mm range of stretch applied to forearm extensor muscles (indicated next to each curve). Each point shows the mean impulse counts (±s.d.) evoked in response to 6 repetitions of the 5 s static component of muscle stretch (of the same form as that represented in A). s.d. fell within the bounds of some symbols here and in other figures.

Figure 2. Amplitude and frequency dependence of ECN neurone responses to muscle vibration

A, impulse traces recorded from an ECN neurone in response to 1 s trains of sinusoidal vibration applied to the EPL muscle, at 10 μm amplitude and frequencies of 50-800 Hz (as indicated), all superimposed on a background 1 mm steady stretch. Bottom trace shows 150 Hz vibration stimulus train. B, mean response (impulses s⁻¹, ±s.d., from 6 responses to 1 s trains of vibration) is plotted as a function of vibration frequency to show the bandwidth of vibration sensitivity at a series of different amplitudes (5, 10, 20, 50 μm peak-to-peak). Impulse counts for the same neurone for which response traces are shown in A.

Figure 4. Bandwidths over which ECN neurones display phase-locked responses to muscle vibration

A-C, R values for up to 8 ECN neurones plotted against muscle vibration frequency at amplitudes of 20, 50 and 100 μm, respectively. The particular forelimb extensor muscle providing input to each neurone is indicated in the legend. Points marked N, including those circled in A were not significantly different from random distributions based on Raleigh's z statistic (see Methods). The 0 Hz value at the origin of the abscissa represents values of R obtained in the absence of vibration. D-F, pooled R values (means ±s.d.) for up to 8 ECN neurones and up to 6 MCN neurones (data from Mackie et al. 1998; see text) as a function of frequency at amplitudes of 20, 50 and 100 μm, respectively. In most cases muscle vibration was superimposed on a 2 mm stretch of muscle (in a few cases muscle stretch was 1 mm). The two groups of neurones (MCN and ECN) were not significantly different at each of the three vibration amplitudes (P≈ 0.18, 0.15, 0.08 for 20, 50 and 100 μm, respectively; Student's paired t test).