INTERACTIONS DURING A CRITICAL PERIOD INHIBIT BILATERAL PROJECTIONS IN EMBRYONIC NEURONS

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 midl ine of the CNS and eventually into the contralateral body wall, thereb y attaining a unilateral pattern of innervation. Certain features of t he adult AP morphology are known to arise through interactions among h omologs early in development (Gao and Macagno, 1987b), but it is not k nown whether the contralateral nature of the projection pattern is due to intrinsic ''one-sidedness'' or rather to cell-cell interactions th at inhibit the formation of a second, ipsilateral projection. In the e xperiments 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 de velopment and then the response of the remaining AP was examined. We f ound that an AP can extend bilaterally symmetrical projections when it s homolog is missing, but only during a critical period that, interest ingly, begins when an AP's interactions with other specific neurons co me to an end. To determine whether synaptic communication between AP h omologs could be responsible for the timing of this critical period, w e recorded electrophysiologically from pairs of embryonic AP neurons. Although no detectable chemical signaling was observed, AP cells mire electrically coupled throughout the entire critical period. Further, t he junctions between these neurons were permeated by 5-HT, whereas lar ger molecules such as carboxyfluorescein were impermeant. This dye cou pling decreased with age even while electrical coupling persisted, sug gesting but not proving that the properties of the gap junctions betwe en AP neurons may also change with time. We conclude that unilateral A P 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.