The interstitial nucleus of Cajal (INC) is thought to control torsional and vertical head posture. Unilateral microstimulation of the INC evokes torsional head rotation to positions that are maintained until stimulation offset. Unilateral INC inactivation evokes head position-holding deficits with the head tilted in the opposite direction. However, the underlying muscle synergies for these opposite behavioral effects are unknown. Here, we examined neck muscle activity in head-unrestrained monkeys before and during stimulation (50 µA., 200 ms, 300 Hz) and inactivation (injection of 0.3 µl of 0.05% muscimol) of the same INC sites. Three-dimensional eye and head movements were recorded simultaneously with electromyographic (EMG) activity in six bilateral neck muscles: sternocleidomastoid (SCM), splenius capitis (SP), rectus capitis posterior major (RCPmaj.), occipital capitis inferior (OCI), complexus (COM) and biventer cervicis (BC). INC stimulation evoked a phasic, short-latency (~5-10 ms) facilitation and later (~100-200 ms) a more tonic facilitation in the activity of ipsi-SCM, ipsi-SP, ipsi-COM, ipsi-BC, contra-RCPmaj. and contra-OCI. Unilateral INC inactivation led to an increase in the activity of contra-SCM, ipsi-SP, ipsi-RCPmaj. and ipsi-OCI, and a decrease in the activity of contra-RCPmaj. and contra-OCI. Thus, the influence of INC stimulation and inactivation were opposite on some muscles (i.e., contra-OCI and contra-RCPmaj.), but the comparative influences on other neck muscles were more variable. These results show that the relationship between the neck muscle responses during INC stimulation and inactivation is much more complex than the relationship between the overt behaviors.