In cultured embryonic chick motoneurons, glutamate-activated currents rise quickly and then decay rapidly to relatively small steady-state current levels. Dopaminergic modulation of these receptors was studied using patch-clamp recording techniques. At concentrations > or = 10 nM, dopamine enhanced glutamate-activated currents by about 200%. This enhancement was diminished by the nonspecific dopamine receptor antagonist S(+)-apomorphine and the more specific D1 receptor antagonist SCH23390, and it was mimicked by the D1 partial agonist SKF38393. Glutamate receptor desensitization rate was not altered in the presence of dopamine. Enhancement was specific to the kainate component. Current-variance analysis indicated that in the presence of dopamine the conductances of glutamate-activated channels were not altered but that the relative fraction of kainate-type channels activated by glutamate increased. Intracellular cAMP levels increased by 33% following exposure to 100 microM dopamine. The effects of elevated cAMP or protein kinase A (PKA) were tested by including 100 microM cAMP or PKA, respectively, in the recording pipette solution. This increased the kainate-activated currents specifically. Dopaminergic enhancement was not observed when a PKA inhibitor was in the pipette. mRNA encoding D1 was detected in the spinal cord by a reverse transcription, polymerase chain-reaction amplification procedure. Thus, dopamine is acting most probably on an avian homolog of the D1 receptor family. We conclude that dopamine causes cAMP to increase, which results in increased activation of kainate-gated channels during glutamate-mediated transmission.