Abstract
Gap junctions between fine unmyelinated axons can electrically couple groups of brain neurons to synchronise firing and contribute to rhythmic activity. To explore the distribution and significance of electrical coupling, we modelled a well analysed, small population of brainstem neurons which drive swimming in young frog tadpoles. A passive network of 30 multicompartmental neurons with unmyelinated axons was used to infer that: axon-axon gap junctions close to the soma gave the best match to experimentally measured coupling coefficients; axon diameter had a strong influence on coupling; most neurons were coupled indirectly via the axons of other neurons. When active channels were added, gap junctions could make action potential propagation along the thin axons unreliable. Increased sodium and decreased potassium channel densities in the initial axon segment improved action potential propagation. Modelling suggested that the single spike firing to step current injection observed in whole-cell recordings is not a cellular property but a dynamic consequence of shunting resulting from electrical coupling. Without electrical coupling, firing of the population during depolarising current was unsynchronised; with coupling, the population showed synchronous recruitment and rhythmic firing. When activated instead by increasing levels of modelled sensory pathway input, the population without electrical coupling was recruited incrementally to unpatterned activity. However, when coupled, the population was recruited all-or-none at threshold into a rhythmic swimming pattern: the tadpole “decided” to swim. Modelling emphasises uncertainties about fine unmyelinated axon physiology but, when informed by biological data, makes general predictions about gap junctions: locations close to the soma; relatively small numbers; many indirect connections between neurons; cause of action potential propagation failure in fine axons; misleading alteration of intrinsic firing properties. Modelling also indicates that electrical coupling within a population can synchronize recruitment of neurons and their pacemaker firing during rhythmic activity.
Highlights
Electrical synapses are widespread in nervous systems from motoneurons to the neocortex and have a long history of study [1,2]
When gap junction blockers were applied, swimming episodes became shorter and descending interneurons (dINs) firing became unreliable, suggesting that the electrical coupling is important for reliable rhythm generation
Our modelling of axo-axonic gap junction coupling in the linear population of tadpole reticulospinal neurons generates a number of predictions that we expect to be relevant to other networks of coupled neurons with fine, unmyelinated axons
Summary
Electrical synapses are widespread in nervous systems from motoneurons to the neocortex and have a long history of study [1,2]. In simpler systems, they have been proposed to reduce response latency, synchronise firing, and detect input coincidence [3,4,5,6,7,8]. To investigate the effect of the gap junctions pharmacological blockers have been used but most are probably non-specific and have effects on other membrane channels [21,27,28,29]. One approach to understanding is through modelling networks of electrically coupled neurons [32]
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