We have examined the role of microtubules (MTs) in the development and maintenance of the cytoplasmic compartmentation of ribosomes in cultured embryonic chick sensory neurons. Control neurons show a sharp cytoplasmic demarcation between the ribosome-rich/MT-deficient 'translational' cytoplasm of the perikaryon and the ribosome-deficient/MT-rich 'expressional' cytoplasm of the axon-like neurites. Neurites treated with 1.0 microgram/ml nocodazole for 15-20 min show in addition to the depolymerization of MTs a clear loss of the cytoplasmic demarcation between the soma and neurite. We found a decreasing density of ribosomes with increasing distance from the soma in the nocodazole treated neurites. Ribosomes, as confirmed by their diameter and sensitivity to ribonuclease treatment, populated the first 100 microns of neurites at roughly the same density as found in the soma (150-300 ribosomes per microns2 in 50 mm longitudinal thin sections). The second 100 microns contained a lower density of ribosomes than the first, 20-60 per microns2, but still higher than controls. Distances past 200 microns were devoid of unambiguous ribosomes. Neurites amputated between 50 and 150 microns from the soma then treated with nocodazole contained a dense population of ribosomes in the proximal segment still attached to the soma, but few or none in the distal segment. We interpret these findings as evidence that ribosomes are able to move from the soma down the neurite after MT disassembly.(ABSTRACT TRUNCATED AT 250 WORDS)