Cell interactions regulate dendritic morphology and responses to neurotransmitters in embryonic chick sympathetic preganglionic neurons in vitro

Abstract

The influence of non-neuronal cells and interneurons on the morphological development of chick sympathetic preganglionic neurons (SPNs) and on the responsiveness of these neurons to the neurotransmitters GABA, glycine, and glutamate was studied. SPNs were retrogradely labeled with the fluorescent dyes dil and diO, then separated from spinal-cord non-neuronal cells and interneurons by fluorescence-activated cell sorting. SPNs were grown in culture, either alone or in coculture with non-neuronal cells alone, with interneurons alone, or with both of these cell types (control cultures). The responsiveness of SPNs to neurotransmitters was assessed by whole-cell recording, while cell morphology was assessed after intracellular staining with 6-carboxyfluorescein. Cell size and morphology were affected by non-neuronal cells. In the absence of non-neuronal cells, SPNs had smaller cell bodies and fewer major processes, whether or not interneurons were present. In contrast, responses to the 3 neurotransmitters were affected by both non-neuronal cells and interneurons, but in ways that differed slightly for each transmitter. In the absence of both non-neuronal cells and interneurons, responses to all 3 transmitters were much smaller than in control cultures, with responses to glutamate most profoundly affected. The addition of either non-neuronal cells or interneurons slightly increased the amplitude of SPN responses to glutamate, but the level of responsiveness with either cell type alone was much lower than for SPNs grown in the presence of both cell types. The addition of interneurons also slightly increased the responsiveness of SPNs to GABA, but non-neuronal cells alone had no significant effect on the responses of SPNs to GABA. Finally, the glycine responsiveness of SPNs was raised to control levels when either non-neuronal cells or interneurons were added. These experiments demonstrate that, though interneurons can have a significant inductive effect on the responses of SPNs to neurotransmitters, not all of the changes in neurotransmitter responsiveness can be related to the formation of functional synapses.

NGF induces neonatal rat sensory neurons to extend dendrites in culture after removal of satellite cells

“…The mechanism by which the satellite cells operate has not been determined. Interestingly, this satellite cell influence on sensory neurons is opposite to the influence of glial cells on neurons that normally extend dendrites in vivo (Tropea et al, 1988;Johnson et al, 1989;Clendening and Hume, 1990); in these latter studies, the presence of glial cells induces dendrite outgrowth. Therefore, with respect to dendrites, these results suggest that, in culture, glial cells influence neurons to acquire properties that they would normally have in vivo.…”

“…Recent studies have indicated that the initiation of dendrites is, in part, governed by mechanisms intrinsic to neurons (Dotti et al, 1988;Black and Baas, 1989). In addition, there is ample evidence that extrinsic factors influence neuronal polarity and dendritic arborization (Mudge, 1984;Bruckenstein and Higgins, 1988a,b;Purves et al, 1988;Snider, 1988;Tropea et al, 1988;Chamak and Prochiantz, 1989;Johnson et al, 1989;Lein and Higgins, 1989;Clendening and Hume, 1990;&hilling et al, 1991).…”

Transplanted Neuroblasts Differentiate Appropriately into Projection Neurons with Correct Neurotransmitter and Receptor Phenotype in Neocortex Undergoing Targeted Projection Neuron Degeneration

“…Multiple previous studies have also reported the expression of differential neurotransmitter and receptor properties by neurons, depending on neuronal surroundings (Clendening and Hume, 1990;Paschen et al, 1997), depolarization, specific neurotransmitters (Patterson, 1978), target tissue interactions (Landis, 1990), glial-neuronal communication (Poulter andBrown, 1999), hormones (McCauley andGee, 1995;Zhang et al, 1999), and neurotrophins (Ernsberger and Rohrer, 1988;Iacovitti et al, 1989;Sieber-Blum, 1991).…”

A developmental handshake: Neuronal control of ionic currents and their control of neuronal differentiation

“…Changes in the response to neurotransmitters can also arise through serial acquisition of sensitivities to more than one transmitter during the course of differentiation, leading to a change in the aggregate response. This process can be regulated postsynaptically, by serial appearance of receptors for different ligands (Clendening and Hume, 1990a), and influenced by the presence of nonneural cells as well as other neurons (Clendening and Hume, 1990b). It may also be regulated presynaptically, by sequential appearance of two or more cotransmitters in other cases.…”