Coding movement direction by burst firing in electrosensory neurons

Abstract

Directional selectivity, in which neurons respond strongly to an object moving in a given direction (“preferred”) but respond weakly or not at all to an object moving in the opposite direction (“null”), is a critical computation achieved in brain circuits. Previous measures of direction selectivity have compared the numbers of action potentials elicited by each direction of movement, but most sensory neurons display patterning, such as bursting, in their spike trains. To examine the contribution of patterned responses to direction selectivity, we recorded from midbrain neurons in weakly electric fish and found that most neurons responded with a combination of both bursts and isolated spikes to moving object stimuli. In these neurons, we separated bursts and isolated spikes using an interspike interval (ISI) threshold. The directional bias of bursts was significantly higher than that of either the full spike train or the isolated spike train. To examine the encoding and decoding of bursts, we built biologically plausible models that examine 1) the upstream mechanisms that generate these spiking patterns and 2) downstream decoders of bursts. Our model of upstream mechanisms uses an interaction between afferent input and subthreshold calcium channels to give rise to burst firing that occurs preferentially for one direction of movement. We tested this model in vivo by application of calcium antagonists, which reduced burst firing and eliminated the differences in direction selectivity between bursts, isolated spikes, and the full spike train. Our model of downstream decoders used strong synaptic facilitation to achieve qualitatively similar results to those obtained using the ISI threshold criterion. This model shows that direction selective information carried by bursts can be decoded by downstream neurons using biophysically plausible mechanisms.