Physiological Properties of Gap Junction Channels in the Nervous System

Before the patch clamp technique was developed, large cells were desirable for the multiple microelectrode impalements that physiological studies of gap junctions required. For that reason, as well as the inherent interest in understanding electrotonic sy

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PHYSIOLOGICAL PROPERTIES OF GAP }UNCTION CHANNELS IN THE NERVOUS SYSTEM David C. Spray 1. INTRODUCTION

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efore the patch clamp technique was developed, large cells were desirable for the multiple microelectrode impalements that physiological studies of gap junctions required. For that reason, as well as the inherent interest in understanding electrotonic synapses, much of the initial characterization of gap junction function, biophysical and pharmacological experiments were performed on the gigantic coupled neurons of molluscs, the fused axons and large cell bodies of arthropod neurons and the identifiable neurons and glia within the segmental ganglia of the leech. A few vertebrate preparations also fulfilled these requirements, such as the giant Mauthner cells 1 and electromotor nuclei of certain teleosts, 2 Rohon-Beard cells in the frog spinal cord 3 and neurons within the inferior olivary nucleus of mammals, 4 but the tedious dissection required for these vertebrate studies led most investigators to pursue the simpler nervous systems of invertebrates. Moreover, 20 years ago a focus of neurobiology was to determine neural circuits in organisms with a limited number of neurons, each of which was identifiable from one animal to the next. 5 If we understood the wiring diagram and activity patterns underlying the brains and behaviors of these animals, it was widely believed, we would progress in large measure toward understanding the human mind. What was learned about the function and physiological properties of electrotonic synapses during this period continues to guide studies on mammalian neurons in tissue culture and in tissue slices, preparations in

Gap junctions in the Nervous System, edited by David C. Spray and Rolf Dermietzel. © 1996 R.G. Landes Company.

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which small cells have been made accessible by a new generation of recording techniques. A major concept that was developed in these invertebrate and lower vertebrate studies is that electrotonic synapses synchronize outputs from coupled cells and provide extraordinarily rapid impulse conduction between pre- and postsynaptic elements, properties that have conveyed evolutionary advantage in certain behavioral repertoires. For example, the rapid impulse propagation between axonal segments in the crayfish and the electrotonic synapses onto motoneurons of both crayfish and hatchetfish allow quick prey evasion by a flip of the tail or pectoral fin; 6•7 coupled presynaptic motoneurons can enable a voracious carnivorous mollusc to synchronously expand its pharynx, ingesting slowly moving prey; 8 and in fish endowed with electric organs the synchrony through electrotonic coupling can provide coordinated output to stun nearby unwary victims. 2 The selective advantage of electrotonic synapses is obvious in these organisms; however, it may not be justifiable to extend these functions to gap junctions in the mammalian nervous system, where junctional expression between adult neurons appears in most cases to be low. The function served by weak or modest coupling