Three-dimensional sensitivity and caudal projection of neck spindle afferents.

1. We recorded from neck muscle spindle afferents in the C2 dorsal root ganglion of the decerebrate cat using floating electrodes. The afferents presumably innervated mainly ventral and ventrolateral perivertebral muscles, and sternocleidomastoid. Stimuli consisted of combinations of rotatory head movements about the roll/pitch or pitch/yaw axes. An important difference from our earlier experiments (10) was the addition of yaw movement to the stimulus paradigm making possible a three-dimensional analysis of afferent behavior. 2. For each afferent we determined the most effective direction of tilt (orientation of the response vector) in three dimensions by using sinusoidal stimuli that combined pitch and roll, or pitch and yaw, or by measuring the gains to responses to roll, pitch, and yaw rotation. 3. Most afferents were sensitive to rotation around all three axes; pitch and yaw were usually more effective than roll. There was no indication of clustering of response vectors, as might be expected if the receptors were located in a small number of muscles each of which has receptors aligned in a homogeneous direction. 4. The responses of afferents were further studied using sinusoidal and trapezoidal stimuli aligned as closely as possible with the orientation of their response vector. The availability of the yaw stimulus made receptor classification based on response linearity, gain, and dynamic index more reliable than in our earlier experiments (10). 5. Muscle spindle responses were divided into three categories: A, B, and ambiguous. The evidence suggests that category A are probably spindle primary receptors and category B are secondaries. Ambiguous receptors have intermediate properties. 6. The caudal projection of spindle afferents was examined by delivering antidromic stimuli with a movable electrode on the surface of the ipsilateral dorsal column. Eighteen percent of the afferents projected to C4, and 14% as far as C5. Long caudal projections can be found in A, B, and ambiguous receptors with a range of directional sensitivities. 7. The evidence suggests that C2 spindle afferents make synapses in the midcervical segments with interneurons and propriospinal neurons that are part of the intraspinal pathway of the tonic neck reflex.