Peripheral target choice by homologous neurons during embryogenesis of the medicinal leech. I. Segment-specific preferences of Retzius cells

Abstract

A pair of large serotonergic neurons, the Retzius (Rz) cells, is found in each segment of the leech nervous system. Most Rz cells innervate the body wall of their own segment as well as adjacent anterior and posterior segments. Rz cells in segments 5 and 6 [Rz (5,6)] instead innervate the reproductive tissue found only in those segments. Rz cells from adjacent segments [Rz (4,7)] provide the serotonergic innervation of the body wall of segments 5 and 6. During embryogenesis, the body wall and the reproductive tissue are apparently available to both Rz (5,6) and Rz (4,7), yet these neurons choose different targets. We asked how Rz (5,6) and Rz (4,7) choose their respective peripheral targets in the reproductive segments by ablating either the reproductive tissue or specific Rz cells. Ablation of the reproductive tissue caused Rz (5,6) to innervate body wall, although not as proficiently as did standard Rz cells, suggesting a preference of Rz (5,6) for reproductive tissue. Ablation of those Rz cells that would normally innervate the body wall of segments 5 and 6 did not cause Rz (5,6) to innervate body wall, ruling out competition for this target. When Rz (5,6) were ablated, Rz (4,7) innervated the body wall of segments 5 and 6 normally and did not innervate reproductive tissue. Thus, competition did not act in the choice of target by Rz (4,7) either. These results suggest that during normal development, Rz (5,6) and Rz (4,7) choose their targets independently of one another rather than competing for the available targets and that these cells have segment-specific target preferences.

Competition among the Axonal Projections of an Identified Neuron Contributes to the Retraction of Some of Those Projections

“…D, Ablating ipsilateral homologs (X ) results in enhanced growth of the longitudinal projections of an AP cell (ϩ), but a diminution of its lateral arborization (Ϫ). , 1989Baptista and Macagno, 1988). Similarly, horizontal axon collaterals of pyramidal cells in the cat striate cortex do not connect precisely to the appropriate target early during development; instead, selective process elimination occurs later when axon collaterals branch extensively within the target area (Callaway and Katz, 1990).…”

Central Synaptic Inputs to Identified Leech Neurons Determined by Peripheral Targets

“…Rz(5,6) become different from their segmental homologs only after contact with their target, the reproductive tissue (5,9,11). Removal of reproductive tissue early in embryogenesis causes Rz (5,6) to develop a central arbor like that of standard Rz cells and to innervate the body wall (3,6). We show here that, after such ablations, the synaptic inputs to Rz(5,6) also develop in a manner appropriate for standard Rz cells.…”

“…3A). Furthermore, Rz (5,6) in these experimental animals were sometimes excited during episodes of swimming (5 of 11 (7) Rz (6) cells (A to C) received excitatory inputs lacking in Rz(5,6) cells (D to F). (7) Rz (7) Rz (6) excited bv tail pinches, (6) is unaffected or slightly inhibited just before and during swimming (2 mV, 2 s).…”

“…IA). Rz cells in most segments innervate the body wall of their own and adjacent segments (4)(5)(6). These neurons modulate the activity of other neurons, glands, and muscles by releasing serotonin (7,8); they receive synaptic inputs from identified cutaneous mechanosensory neurons and from neurons that generate the swimming motor program (8)(9)(10).…”

“…These neurons modulate the activity of other neurons, glands, and muscles by releasing serotonin (7,8); they receive synaptic inputs from identified cutaneous mechanosensory neurons and from neurons that generate the swimming motor program (8)(9)(10). In contrast, Rz cells in segments 5 and 6 [Rz (5,6)] innervate the reproductive tissue, which is found only in those segments (5,9,11); these neurons do not receive the same synaptic inputs as their standard segmental homologs (9,10). Although there are a number of morphological and physiological differences among mature Rz cells, all Rz cells early in their development have similar central and peripheral projections (9,11).…”