Motoneurons of the oculomotor nucleus subserving multiply innervated muscle fibres (MIF) receive different afferent inputs from the motoneurons subserving singly innervated muscle fibres (SIF). We asked whether MIF and SIF motoneurons have different neurotransmitter signalling expression profiles. Adult rhesus monkey extraocular muscles were injected with the retrograde tracer cholera toxin. Sections were then stained for various neurotransmitter-signalling markers. MIF motoneurons showed less glutamate receptor 4 (GluR4) and N-methyl-d-aspartate receptor 1 (NMDAR1) immunoreactivity, but showed similar amounts of glutamic acid decarboxylase (GAD) immunoreactive afferent terminals, compared to SIF motoneurons. This difference in excitatory neurotransmitter receptor expression may explain selective oculomotor deficits and allow development of selective pharmacotherapy in the future.