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

Abstract

1. The capacity of cuneate neurones to signal information derived from muscle spindle afferent fibres about static stretch or vibration of forearm extensor muscles was examined electrophysiologically in anaesthetized cats. 2. Static stretch (>= 2 mm in amplitude) and sinusoidal vibration (at frequencies of 50-800 Hz) were applied longitudinally to individual muscle tendons by means of a feedback controlled mechanical stimulator, and responses were recorded from individual cuneate neurones and from individual spindle afferent fibres. 3. Cuneate neurones sampled were located caudal to the obex and displayed a sensitivity to both vibration and static stretch of forearm muscles that was consistent with their input arising from primary spindle endings. In response to static muscle stretch, they displayed graded and approximately linear stimulus-response relations, and a stability of response level at fixed lengths that was consistent with these neurones contributing discriminative information about static muscle stretch. 4. In response to sinusoidal muscle vibration the cuneate neurones also showed graded stimulus-response relations (in contrast to spindle afferents which at low vibration amplitudes attain a plateau response level corresponding to a discharge of 1 impulse on each vibration cycle). Lowest thresholds were at 100-300 Hz and bandwidths of vibration sensitivity extended up to approximately 800 Hz. 5. Temporal precision in cuneate responses to muscle vibration was assessed by constructing phase scatter and cycle histograms from which measures of vector strength could be calculated. Cuneate responses displayed somewhat poorer phase locking (and lower vector strengths) than spindle afferent responses to vibration (a reflection of uncertainties associated with synaptic transmission). Nevertheless, the remarkable feature of cuneate responses to muscle vibration is the preservation of tight phase locking at frequencies up to 400-500 Hz, which presumably enables these central neurones to contribute accurate temporal information for the kinaesthetic sense in a variety of circumstances involving dynamic perturbations to skeletal muscle.

Figure 7. Effect of vibration amplitude on phase locking of spindle afferent (A-C) and cuneothalamic neurone (D-F) responses to muscle vibration

Phase scatter graphs (left side) and cycle histograms (right side) constructed from responses of a spindle afferent fibre (A-C) and cuneothalamic neurone (D-F) to six repetitions of a 1 s train of vibration applied to the muscle tendon (IPr muscle in A-C; EDL in D-F; 150 Hz vibration, amplitudes indicated in each cycle histogram). Phase scatter graphs display the time of each impulse occurrence (single dot) 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 the phase scatter graphs and display the cumulative distribution of impulse occurrences within the vibration stimulus cycle (abscissa is number of impulse counts in each of the 50 time addresses into which the 6.7 ms ordinate scale was divided).

Figure 9. Effect of vibration frequency on phase locking of spindle afferent (A-C) and cuneate neurone (D-F) responses to muscle vibration

Phase scatter graphs and cycle histograms constructed from responses of representative spindle afferent fibre (A-C) and a cuneothalamic neurone (D-F) to six repetitions of 1 s trains of vibration (10 μm amplitude, A-C; 50 μm, D-F) applied at three frequencies (150 Hz in A and D, 300 Hz in B and E, 500 Hz in C and F). Format as in Fig. 7, except ordinates in A and D, B and E, and C and F, correspond to vibration cycle periods of 6.7 ms, 3.3 ms and 2.0 ms, respectively.

Figure 1. Capacity of cuneate neurones to respond to static muscle stretch

A 2 mm ramp-and-hold stretch lasting 5 s (0.5 s onset and offset ramps; waveform at top) generated a maintained response reflected, first, in the impulse record (large spike, ∼1 mV peak-to-peak amplitude; negativity upwards here and in other response traces), second, in the peristimulus time histogram (constructed from 6 successive responses; address width, 80 ms), and third, in the instantaneous frequency plot (lowest panel). The neurone was identified as a cuneothalamic projecting neurone according to criteria described in Methods.

Figure 3. The capacity of cuneate neurones and spindle afferent fibres to respond to muscle vibration superimposed upon static stretch of the muscle

Impulse records and peristimulus time histograms (constructed from 6 consecutive responses; address width, 80 ms) for a representative spindle afferent fibre (A and B) and cuneothalamic neurone (C and D) activated by both static muscle stretch (1 mm amplitude, 5 s duration) and sinusoidal vibration (150 Hz, 1 s duration starting 3 s after onset of stretch; amplitude, 20 μm for A and B, 25 μm for C and D) applied to the muscle tendon (vibration amplitude is exaggerated on stimulus waveform in upper trace for purposes of illustration). Spike height in A, 0.5 mV; in B, 2.6 mV.

Figure 2. Stimulus-response relations for five cuneate neurones responsive to static stretch of forearm extensor muscles

The neurones exhibited a graded response as a function of static stretch amplitude over the 2 mm range tested. Each point represents the mean (±s.d.) impulse count in six consecutive responses to the 5 s static stretch of different extensor muscles. (s.d. fell within the bounds of some symbols here and in other figures.) The top four labelled curves were from neurones tested and confirmed as cuneothalamic projecting neurones.

Figure 4. Amplitude dependence of responses to muscle vibration in representative spindle afferent fibre (A) and cuneothalamic neurone (B)

Vibration at 150 Hz (1 s duration) was applied longitudinally to the muscle tendon. The primary afferent attained a plateau 1 : 1 response level at ∼10 μm whereas the cuneate neurone response was graded up to 150-200 μm. Vibration was superimposed on a 2 mm stretch of each muscle (cf. Fig. 3) applied from a low background tension of ∼5-10 g wt. Spike heights, ∼0.5 mV (A) and 1 mV (B).

Figure 5. Stimulus-response relation (A) and bandwidth of vibration sensitivity (B) for a representative muscle spindle afferent fibre

A, mean response (impulses s⁻¹±s.d.; n = 6) as a function of vibration amplitude for five vibration frequencies (50-800 Hz) applied in 1 s trains to the muscle tendon. In B the mean response is replotted as a function of vibration frequency to show the bandwidth of vibration sensitivity at five different vibration amplitudes.

Figure 6. Stimulus-response relation (A) and bandwidth of vibration sensitivity (B) for a representative cuneothalamic neurone

A, mean response (impulses s⁻¹±s.d.; n = 6) as a function of vibration amplitude for seven vibration frequencies (50-800 Hz) applied in 1 s trains to the muscle tendon. B, mean response is replotted as a function of vibration frequency to show the bandwidth of vibration sensitivity at a series of different amplitudes.

Figure 8. Quantitative comparison of the capacities of spindle afferents and cuneate neurones to display phase locked responses to muscle vibration

A, resultant values for responses of a muscle afferent fibre to muscle vibration at frequencies in the range 50-800 Hz and at amplitudes up to 150 μm. B, resultant values for responses of a cuneothalamic neurone to muscle vibration frequencies in the range 50-800 Hz and at amplitudes up to 200 μm.

Figure 10. Quantitative comparison of the frequency bandwidths over which spindle afferents and cuneate neurones display phase locked responses to muscle vibration

Resultant values plotted as a quantitative measure of phase locking in the responses to muscle vibration of a spindle afferent fibre (A) and cuneothalamic neurone (B) as a function of vibration frequency for a range of different amplitudes.

Figure 11. Frequency bandwidths over which cuneate neurones display phase locked responses to muscle vibration

The three graphs plot the values of the resultant for six cuneate neurones as a function of vibration frequency at three different amplitudes of the muscle vibration (20, 50 and 100 μm). The bottom four of the six labelled curves (APL, EDL, ECRB and EDC) were obtained from neurones tested and identified as cuneothalamic projecting neurones.