Abstract In this study, fast synaptic transmission at vertebrate CNS connections mediated by several different nicotinic ACh receptors (nAChRs) was investigated with paired recordings from pre‐ and postsynaptic neurons. Analysis of the response kinetics at the axo‐axonic connections between the Mauthner (M‐) axon and cranial relay neurons (CRN) indicates up to three main components are present and can be characterized by fast, ∼1.5 ms, intermediate, ∼6 ms and slow, ∼15 ms, decay time constants. Further analysis indicates most responses have multiexponential decays and each response falls into one of six classes dependent on the weight and combination of kinetic components. Pharmacological results suggest that up to three nAChRs, α7*, α3β2* and α3β4*, mediate the postsynaptic responses and correspond to the fast, intermediate and slow decay components, respectively. The fast decay component is blocked by ∼35 nm methyllycaconitine (MLA), 100 nmα‐bungarotoxin (α‐Btx) or 150 nmα‐conotoxin (α‐Ctx) ArIB. The intermediate decay component is blocked by 2 μm dihydro‐beta‐erythroidine (DHβE) or 200 nmα‐Ctx GIC. The slow decay component is blocked by 10 μmα‐Ctx AuIB, but not by 7.25 μm DHβE. Intriguingly, the mEPSPs (minis) at connections with evoked EPSPs best fitted by multiple exponentials, were not composite; rather, there were multiple populations of minis, each with single exponential decay times corresponding to those of the different evoked EPSP components. This indicates that the different receptors are topographically segregated at the connection between the M‐axon and CRN axon. These results suggest that, as with glutamate, fast nicotinic synaptic transmission in the CNS can be mediated by multiple receptors in the same postsynaptic neuron. The coexistence of EPSPs of different durations may have implications for network function and plasticity.