The anterior pagoda (AP) neurons in the CNS of the medicinal leech are found as homologous pairs in 20 of the 21 midbody ganglia. Each AP is the mirror image of its mate, extending its main axon across the midline of the CNS and eventually into the contralateral body wall, thereby attaining a unilateral pattern of innervation. Certain features of the adult AP morphology are known to arise through interactions among homologs early in development (Gao and Macagno, 1987b), but it is not known whether the contralateral nature of the projection pattern is due to intrinsic “one-sidedness” or rather to cell-cell interactions that inhibit the formation of a second, ipsilateral projection. In the experiments described in this report, we tested the possibility that an AP's contralateral homolog itself inhibits the formation of bilateral projections. One AP was photoablated in the intact embryo early in development and then the response of the remaining AP was examined. We found that an AP can extend bilaterally symmetrical projections when its homolog is missing, but only during a critical period that, interestingly, begins when an AP's interactions with other specific neurons come to an end. To determine whether synaptic communication between AP homologs could be responsible for the timing of this critical period, we recorded electrophysiologically from pairs of embryonic AP neurons. Although no detectable chemical signaling was observed, AP cells were electrically coupled throughout the entire critical period. Further, the junctions between these neurons were permeated by 5-HT, whereas larger molecules such as carboxyfluorescein were impermeant. This dye coupling decreased with age even while electrical coupling persisted, suggesting but not proving that the properties of the gap junctions between AP neurons may also change with time. We conclude that unilateral AP cells possess the intrinsic ability to project bilaterally, but are inhibited from doing so by age- dependent interactions with homologous neurons, possibly mediated by gap-junctional communication.