1. The role of tetrodotoxin (TTX)-sensitive (Na+) channels in the generation of antidromic and orthodromic field potentials of the CA1 pyramidal cell population was examined by local application of TTX in the in vitro rat hippocampal slice preparation. 2. The sensitivity of alvear (antidromic) and stratum oriens (SO)-evoked potentials to TTX application (10-100 microM) was tested in stratum pyramidale and over the entire extent of pyramidal cell apical dendrites in stratum radiatum. Stratum radiatum (SR)-evoked potentials were examined at the level of pyramidal cell bodies and over the proximal 200 microns of the apical dendritic region. 3. Pressure application of TTX confined to stratum pyramidale or regions of stratum radiatum selectively blocked the negative component of antidromic and SO-evoked population discharge in the cell body layer and over the initial 200 microns of stratum radiatum. 4. SR stimulation evoked a complex field potential in the proximal stratum radiatum (less than 150 microns) composed of at least three components: 1) A short-duration (approximately 3 ms) negativity of shorter peak latency than the population spike recorded simultaneously in stratum pyramidale. This potential was highly sensitive to TTX and appeared to be instrumental in the generation of the cell body population response. 2) A long-duration negativity (approximately 20 ms) evoked at stimulation strengths that were subthreshold for both the short-duration negativity in proximal stratum radiatum and the cell body population spike. Although apparently less sensitive to TTX, this potential was reduced in amplitude with repeated TTX application; and 3) a slow (approximately 12 ms) positive-going potential that was only observed after eliminating all TTX-sensitive conductance mechanisms in the proximal stratum radiatum. 5. The latency difference between the SR-evoked short-duration negativity of proximal stratum radiatum and the population spike in stratum pyramidale decreased or reversed during the course of multiple discharge induced by the addition of bicuculline or picrotoxin (5-10 microM) to the perfusate. 6. These data indicate the presence of TTX-sensitive presumed Na+ channels over the initial 200 microns of pyramidal cell apical dendrites capable of supporting active conduction of population discharge evoked by antidromic or SO stimulation. The sensitivity of SR-evoked potentials to TTX suggests that a synaptic potential generated in the distal apical dendrites is capable of triggering both a slow active depolarization and a fast spike-like discharge in the proximal apical dendritic region.(ABSTRACT TRUNCATED AT 400 WORDS)