Ectopic sensory neurons in mutant cockroaches compete with normal cells for central targets

Abstract

The cercus of the first instar cockroach, Periplaneta americana, bears two filiform hairs, lateral (L) and medial (M), each of which is innervated by a single sensory neuron. These project into the terminal ganglion of the CNS where they make synaptic connections with a number of ascending interneurons. We have discovered mutant animals that have more hairs on the cercus; the most typical phenotype, called “Space Invader” (SI), has an extra filiform hair in a proximo-lateral position on one of the cerci. The afferent neuron of this supernumerary hair (SIN) “invades the space” occupied by L in the CNS and makes similar synaptic connections to giant interneurons (GIs). SIN and L compete for these synaptic targets: the size of the L EPSP in a target interneuron GI3 is significantly reduced in the presence of SIN. Morphometric analysis of the L afferent in the presence or absence of SIN shows no anatomical concomitant of competition. Ablation of L afferent allows SIN to increase the size of its synaptic input to GI3. Less frequently in the mutant population, we find animals with a supernumerary medical (SuM) sensillum. Its afferent projects to the same neuropilar region as the M afferent, makes the same set of synaptic connections to GIs, and competes with M for these synaptic targets. The study of these competitive interactions between identified afferents and identified target interneurons reveals some of the dynamic processes that go on in normal development to shape the nervous system.