Electrical excitability: A spectrum of properties in the progeny of a single embryonic neuroblast

Abstract

We have examined the range of some properties of the progeny of a single embryonic precursor cell in the grasshopper. The t100 progeny of this single neuroblast share certain features such as their transmitter and some aspects of their morphology; at the same time, however, they demonstrate a broad spectrum of electrical properties, from spiking to nonspiking neurons. The first-born progeny are spiking neurons with peripheral axons. Many of the progeny, including all of the last-born, do not generate action potentials. The nonspiking progeny are local intraganglionic neurons and appear to compose a majorproportion of the progeny of this neuroblast. All of the nonspiking neurons have calcium inward current channels and can make action potentials when outward current channels are blocked. We propose a model for grasshopper neurogenesis based on cell lineage such that'(i) certain features (e.g., transmitter) are shared by the progeny of all cell divisions from a single neuroblast, and (ii) other features (e.g., electrical properties) are shared by the pro eny of a given birth position (e.g., first versus last born) from all of the neuroblasts. According to this model, the first-born progeny from all neuroblasts are spiking neurons, whereas the last-born are nonspiking.We have been studying the embryonic development of identified neurons in grasshoppers (1-4). Individually identified neurons are sufficiently large in grasshopper embryos to permit visualization with a compound microscope and impalement with intracellular microelectrodes from the time of their birth to their maturation. Our studies thus far have sought to describe the temporal pattern of differentiation from an identified neuroblast (precursor cell) to a group of identified neurons.Each thoracic segment in the embryo contains over 60 precursor cells that give rise to the roughly 3000 neurons of each thoracic ganglion (5). The subjects of our studies have been the dorsal unpaired median (DUM) neurons, whose t100 somata form a distinct cluster on the dorsal midline of each segmental ganglion (6-8). A single embryonic precursor cell, the median or DUM neuroblist, gives rise to most of the DUM neurons (1); two of them are the progeny of another precursor cell, MP3 (3,4). In an adult thoracic ganglion, only six to eight of the DUM neurons have large-diai~eter somata; most are much smaller. Previous physiological studies on adult DUM neurons focused on the few cells with large somata and described these cells as having spiking somata and spiking axons (9, 10). Our previous embryonic studies described the temporal sequence of differentiation of the three oldest progeny of the DUM neuroblast; these cells develop into three of the largest DUM neurons and all have spiking somata and spiking axons (1, 2).In the present study, we have sampled the range of physiological properties of the t100 progeny of the DUM neuroblast, from the oldest to the youngest and from the biggest to the smallest. What' properties are common to all or many of the progeny, and wh...