The medial vestibular nucleus (MVN) and prepositus hypoglossi nucleus (PHN) neurons receive cholinergic inputs from the pontomesencephalic reticular formation. Such inputs are thought to play important roles in horizontal eye movements. We previously found that the nicotinic ACh receptors (nAChRs)-mediated current responses were larger than those muscarinic ACh receptors (mAChRs)-mediated responses in cholinergic neurons that projected to the cerebellum, suggesting the predominant expression of nAChRs in the neurons. In this study, we clarified whether the expression patterns of ACh receptors are different in neurons exhibiting distinct neurotransmitter phenotypes using whole-cell recordings in brainstem slices. Individual neuron types such as cholinergic, GABA/glycinergic, and putative glutamatergic neurons were identified using specific transgenic rats. We first investigated the cholinergic current responses to the puff application of ACh in the three neuron types. We found that the nAChR-mediated currents were also larger than mAChR-mediated currents in all three types of neurons. When the nAChR-mediated currents were isolated by the application of mAChR antagonist, atropine, three types of nAChR-mediated current responses that exhibited the distinct activation and desensitization kinetics were detected, and therefore they were designated as fast, slow, and fast & slow types. The fast type was a preferred response in both MVN and PHN GABA/glycinergic neurons, while the slow type was a preferential response in both MVN and PHN glutamatergic neurons. The cholinergic neurons showed no preferred response type. Pharmacological analyses revealed that the fast, slow, and fast & slow types were mainly mediated by α7, non-α7, and both α7 and non-α7 nicotinic receptors, respectively. These findings suggest that MVN and PHN neurons express nAChRs predominantly and show three distinct current responses dependent on the expressions of α7 and/or non-α7 receptors. Furthermore, the proportions of neurons exhibiting these three response types may be different in the neuron types.