1. We have investigated the developmental expression of three voltage-gated K currents on neonatal rat superior cervical ganglion (SCG) neurons in vivo and in culture: a rapidly inactivating current (IAf), a slowly inactivating current (IAs), and a noninactivating current (IK). 2. On postnatal day 1 neurons (P1), mean peak IAs is 67 +/- 4 (SE) pA/pF, peak IAf is 27 +/- 3 pA/pF, and IK is 14 +/- 3 pA/pF. Over the next wk, there is a switch in the expression of these currents: IAs drops by 40%, whereas IAf increases by greater than 100%; there is no change in IK. On P14 neurons, IAs is 38 +/- 2 pA/pF, IAf is 64 +/- 5 pA/pF, and IK is 12 +/- 1 pA/pF. 3. The change in expression of K currents on SCG neurons over the first 2 postnatal wk is unaffected by preganglionic innervation or by innervation of the targets. 4. To learn more about the factors that affect K current expression on these neurons, we grew SCG neurons in culture without other cell types for various times, and we measured the expression of IAf, IAs, and IK. In culture, the currents remained at their P1 levels for the first 4-7 days. Thereafter, both IAs and IAf decreased to low levels over a period of 2-3 wk. These results suggest that an epigenetic factor(s) is necessary for the expression of IAf and IAf in vivo and that this factor is missing in culture. 5. When IAs and IAf decreased on neurons in culture, we observed a compensatory increase in IK. After 4 wk in culture, IK is fourfold greater than on neurons in vivo. This result suggests that these neurons have intrinsic mechanisms that coordinate the expression of different voltage-gated K currents.