MORMYROMAST ELECTRORECEPTOR ORGANS AND THEIR AFFERENT-FIBERS IN MORMYRID FISH .2. INTRAAXONAL RECORDINGS SHOW INITIAL-STAGES OF CENTRAL PROCESSING

Physiologically and morphologically identified primary afferent fibers from mormyromast electroreceptor organs were recorded intracellularly. The fiber recordings were made from the nerve root of the posterior lateral line nerve, where the fibers enter the brain, and from the electrosensory lateral line lobe (ELL), near the central termianls of the fibers. The intracellular recordings reveal a variety of potentials, synaptic and nonsynaptic, in addition to the large orthodromic action potentials from the periphery. The goal of the present study was to describe and interpret these various potentials in mormyromast afferent fibers as a first step in understanding the processing of electrosensory information in ELL. Three types of synaptic potentials were recorded inside mormyromast afferent fibers: 1) electric organ corollary discharge (EOCD) excitatory postsynaptic potentials (EPSPs), driven by the motor command that elicits the electric organs discharge (EOD); 2) EPSPs evoked by electrosensory stimulation of electroreceptors in the skin near the electroreceptor from which the recorded fiber originates or by direct stimulation of an electrosensory nerve; and 3) inhibitory postsynaptic potentials (IPSPs) evoked by electrosensory stimulation of more distant electroreceptors. These synaptic potentials can be attributed to synaptic input to postsynaptic cells in ELL that is observed inside the afferent fibers because of electrical synapses between the fibers and the postsynaptic cells. The peripherally evoked EPSPs could frequently be shown to be unitary. The unitary EPSPs were identical to the orthodromic spikes in originating from a single electroreceptor, in threshold, and in latency shift with increasing stimulus intensity. These similarities suggest that the unitary EPSPs are electrotonic EPSPs caused by impulses in other mormyromast afferent fibers that terminate on some of the same postsynaptic cells as the recorded fiber. The peripherally evoked IPSPs had a longer latency than the EPSPs or orthodromic spikes, requiring the presence of an inhibitory interneuron. The peripherally evoked EPSPs, both unitary and nonunitary, show absolute refractory periods of 3-8 ms, followed by relative refractory periods of ~8 ms, when tested with two identical stimuli to a nerve. These refractory periods are interpreted as because of refractoriness in the fine preterminal branches of the axonal arbor. A depolarizing afterpotential is commonly associated with the orthodromic spike and probably results from the successful propagation of the spike into the entire terminal arbor. The depolarizing afterpotential has a refractory period that is similar to that of the peripherally evoked EPSPs and that is also interpreted as refractoriness in the fine preterminal branches. Small spikes or spikelets often arise from large peripherally evoked EPSPs or from the summation of peripherally evoked EPSPs and EOCD EPSPs. With further depolarization, the small spikes often give rise to full-sized spikes of the same size as the orthodromic spikes. Several results indicate that the spikelets are action potentials in restricted parts of the axonal arbor that do not propagate into the parent axon, and that the full-sized spikes arising from the spikelets or EPSPs are antidromic spikes in the parent axon that are propagated out of the periphery. In conclusion, this study provides information about some initial processes in the analysis of electrosensory information, including corollary discharge excitation, convergence of afferent signals, and surround inhibition. The results are also relevant to the general issue of impulse propagation in axonal arbors. The peripherally evoked EPSPs and depolarizing afterpotentials probably reflect impulse propagation into the terminals of an axonal arbor. The results suggest that postimpulse refractoriness in fine preterminal branches is a major limiting factor for such orthodromic propagation. The spikelets and antidromic spikes, however, appear to reflect impulses initiated in the terminals and propagated in the opposite direction. The results suggest that branch point failure may be a limiting factor in this antidromic direction.