Neuronal coincidence detection by voltage-sensitive electrical synapses

Abstract

Coincidence detection is important for functions as diverse as Hebbian learning, binaural localization, and visual attention. We show here that extremely precise coincidence detection is a natural consequence of the normal function of rectifying electrical synapses. Such synapses open to bidirectional current f low when presynaptic cells depolarize relative to their postsynaptic targets and remain open until well after completion of presynaptic spikes. When multiple input neurons fire simultaneously, the synaptic currents sum effectively and produce a large excitatory postsynaptic potential. However, when some inputs are delayed relative to the rest, their contributions are reduced because the early excitatory postsynaptic potential retards the opening of additional voltage-sensitive synapses, and the late synaptic currents are shunted by already opened junctions. These mechanisms account for the ability of the lateral giant neurons of crayfish to sum synchronous inputs, but not inputs separated by only 100 sec. This coincidence detection enables crayfish to produce ref lex escape responses only to very abrupt mechanical stimuli. In light of recent evidence that electrical synapses are common in the mammalian central nervous system, the mechanisms of coincidence detection described here may be widely used in many systems.Despite the importance of coincidence detection in many systems (1), including Hebbian learning (2-4), binaural localization (5-7), and visual attention (8, 9), the cellular mechanisms responsible for such detection are not well understood. Brevity of transmitter action, short postsynaptic membrane time constants, and rapidly activating outward currents that are triggered by excitatory postsynaptic potentials (EPSPs) can contribute to selective responsiveness to coincident stimuli (10-13). We report here that the properties of rectifying electrical synapses enable precise coincidence detection by a postsynaptic neuron that receives excitatory inputs from a converging array of these synapses. Coincidence detection is therefore an emergent property of rectifying synapses in a convergent network. Converging networks of this kind are realized in the afferent pathway to the lateral giant (LG) neuron of the crayfish, a command neuron for a tail flip escape reaction. We found that this network displays the predicted high degree of selection for coincident inputs. METHODS Theoretical.Each model neuron is a single electrical compartment with Hodgkin-Huxley conductances (14), and an electrical rectifier (Fig. 1A, diode symbol) with a voltage dependence similar to that of the giant motor synapse of crayfish (15, 16). For both model neurons, G NaMax ϭ 720 S, G KMax ϭ 216 S, G L ϭ 1 S, E Na ϭ ϩ45 mV (relative to a Ϫ70 mV rest potential), E K ϭ Ϫ82 mV, E L ϭ Ϫ60 mV, and C (compartmental capacitance) ϭ 6 nF. These values are equivalent to those of the Hodgkin-Huxley model of the squid axon calculated for a temperature of 19°C and are not critical for the operation of the model. For the rectifying elect...

A mechanism for neuronal coincidence revealed in the crayfish antennule

“…In a typical adult crayfish antennule that is 2.5 cm long, and assuming a mean axonal conduction velocity of 3 m/sec, differences in spike arrival time at the brain (an additional 1-cm long pathway proximal to the flagellar bases) from sensilla at the base of a flagellum and from those near the tip could be as large as 8.5 msec. This latency difference could obviate coincident spike arrival and compromise the kind of electrical interactions between central afferent terminals that are so important for activation of the lateral giant system (11,12). Interestingly, however, we found that response latencies of spikes generated from sensilla near the tip of the antennular flagella and those generated near the flagellar base differ only by 1.0-1.5 msec recorded at the base.…”

“…The neurophysiological substrates of startle behaviors include interneuron axons of very large diameters that conduct impulses rapidly to excite relevant efferent pathways (1)(2)(3)(4)(5) and electrical synapses in the sensory-afferent pathways that trigger the interneurons and, in some systems, the motor neurons involved in the behavior (6). One of the startle behaviors that has been most intensively studied is a tailflip reflex initiated by one of the two sets of these high-speed interneurons-the lateral giant fibers-in the ventral nerve cord of crayfish (7)(8)(9)(10)(11)(12). Rectifying electrical synapses between sensory-afferent terminals and the lateral giant fibers and between large tactile interneurons and the lateral giants, passes current directly into these paired axons and, when several afferent terminals fire simultaneously, they sum effectively to produce enhanced excitatory postsynaptic potentials in their targets (11).…”

“…One of the startle behaviors that has been most intensively studied is a tailflip reflex initiated by one of the two sets of these high-speed interneurons-the lateral giant fibers-in the ventral nerve cord of crayfish (7)(8)(9)(10)(11)(12). Rectifying electrical synapses between sensory-afferent terminals and the lateral giant fibers and between large tactile interneurons and the lateral giants, passes current directly into these paired axons and, when several afferent terminals fire simultaneously, they sum effectively to produce enhanced excitatory postsynaptic potentials in their targets (11). Furthermore, nonrectifying electrical interconnections among the afferent terminals exist whereby active terminals can directly recruit inactive terminals to provide additional depolarization to the lateral giants (12).…”

Neuronal competition for action potential initiation sites in a circuit controlling simple learning

“…The sensory-and S-cells all excite the L-motoneurons (Muller, 1979). Although the S-cell differs from other giant axons because it is not itself able to generate significant shortening of the animal (Gardner-Medwin et al, 1973), input to the L-motoneuron from the S-cell coincident with sensory-cell input may enhance the motoneuron's response, similar to an effect observed in the crayfish escape circuit (Edwards et al, 1998). Thereby, the S-cell may strengthen shortening during sensitization.…”

Recovering real-world images from single-scale boundaries with a novel filling-in architecture

“…voltage dependent) gap junctions (e.g. Edwards, Heitler, Leise, & Friscke, 1991;Edwards, Yeh, & Krasne, 1998). BEATS filling-in is now introduced formally, with parameter values given in Table 2.…”