Human neck muscles have a complex multi-layered architecture. The role and neural control of these neck muscles were examined in nine seated subjects performing three series of isometric neck muscle contractions: i) 50 N contractions in eight fixed horizontal directions, ii) 25 N contractions and iii) 50 N contractions, both with a continuously changing horizontal force direction. Activity in the left sternocleidomastoid, trapezius, levator scapulae, splenius capitis, semispinalis capitis, semispinalis cervicis and multifidus muscles was measured with wire electrodes inserted at the C4/C5 level under ultrasound guidance. We hypothesized that deep and superficial neck muscles would function as postural and focal muscles respectively, and would thus be controlled by different neural signals. To test these hypotheses, EMG tuning curves and correlations in the temporal and frequency domains were computed. Three main results emerged from these analyses: i) EMG tuning curves from all muscles exhibited well-defined preferred directions of activation for the 50N isometric forces, ii) larger contractions (25 vs. 50N) yielded more focussed EMG tuning curves and iii) agonist neck muscles from all layers received a common neural drive in the range of 10-15 Hz. The current results demonstrate that all neck muscles can exhibit phasic activity during isometric neck muscle contractions. Similar oscillations in the EMG of neck muscles from different layers further suggest that neck motoneurons were activated by common neurons. The reticular formation appears a likely generator of the common drive to the neck motoneurons due to its widespread projections to different groups of neck motoneurons.