Changes in human muscle spindle sensitivity during a proprioceptive attention task

Abstract

The aim of the present study was to test whether fusimotor control of human muscle spindle sensitivity changed when attention was selectively directed to the recognition of an imposed two-dimensional movement in the form of a written symbol. The unitary activities of 32 muscle spindle afferents (26 Ia, 6 II) were recorded by microneurography at the level of the common peroneal nerve. The patterns of firing rate in response to passive movements of the ankle, forming different letters or numbers, were compared in two conditions: control and recognition. No visual cues were given in either condition, but subjects had to recognize and name the character in one condition compared with not paying attention in the control condition. The results showed that 58% of the tested Ia afferents presented modified responses to movements when these had to be recognized. Changes in Ia afferent responses included decreased depth of modulation, increased variability of discharge, and changes in spontaneous activity. Not all changes were evident in the same afferent. Furthermore, the percentage of correctly recognized movements amounted to 63% when changes were observed, but it was only 48% when the primary ending sensitivity was unaltered. The responses of group II afferents were only weakly changed or unchanged. It is suggested that the altered muscle spindle sensitivity is because of selective changes in fusimotor control, the consequence of which might be to feed the brain movement trajectory information that is more accurate.

Figure 1.

Examples of responses to ramp, hold (left), and sinusoidal (right) movements used to classify the afferent as primary (upper part) or secondary (lower part). Each part of the figure panels represents, from bottom to top, the imposed movement, the unitary activity, and the corresponding instantaneous discharge frequency curve. Imp, Impulse.

Figure 2.

Responses of a primary muscle spindle afferent to imposed writing-like movements during a full control session. Primary afferent activity from the EDL muscle recorded during a control session of imposed movements is illustrated by its spike train and the corresponding instantaneous discharge frequency curve. Each graphic symbol is represented by the displacement along the horizontal (x) and vertical (y) axis. The flat electrodermal (on top) and EMG (on bottom) recordings reflect the mentally and physically relaxed states of the subject. Note that each graphic symbol (between the vertical dotted lines) corresponds to a highly specific Ia firing pattern. Imp, Impulse.

Figure 3.

Reproducibility of the primary afferent responses to successive imposition of the same writing movement during control. Examples of responses of an Ia afferent belonging to the EDL muscle to six successive impositions of the movement forming the cursive letter “b.” Represented from bottom to top are the x and y coordinates of the movement, the unitary activity with its corresponding instantaneous frequency curve, and the responses of the same afferent recorded during each of the five other successive movements illustrated by related instantaneous frequency curves. Imp, Impulse.

Figure 4.

Example of the increased variability of the instantaneous frequency of Ia afferents during recognition compared with control. During control and recognition sessions (top and bottom part, respectively), the responses of an Ia afferent from the EDL muscle (unit 5) (Table 1) to imposed movement forming the word “in” are illustrated. Each part of the figure, from top to bottom, illustrates the instantaneous frequency curve and spike train, the imposed movement represented by its x and y coordinates, and EMG activity of the receptor-bearing muscle. Imp, Impulse.

Figure 5.

Example of the decreased dynamic sensitivity of muscle spindle primary endings during recognition compared with control. Same legend as in Figure 4, except that the Ia afferent (unit 3) (Table 1) rose from the PL muscle and that the trajectory of the imposed movements drew the letter “m.” Imp, Impulse.

Figure 6.

Example of slight changes in the response of group II afferents. Same legend as in Figure 4, except that the secondary afferent belonged to the TA muscle and the trajectory of the imposed movement drew the word “in.” Imp, Impulse.

Figure 7.

Characterization of the Ia afferent responses by the VI. A, The responses of the Ia afferent, previously shown on Figure 4, were filtered using a Hanning window (see Materials and Methods) during control (gray symbols and curve) and recognition (black symbols and curve). The VIs are given on the upper right part. Note that the VI increases during recognition. B, Same as in A, with the responses of Ia afferent previously shown in Figure 5. Note that VI decreases during recognition.