Timing Actions to Avoid Refractoriness: A Simple Solution for Streaming Sensory Signals

Abstract

Segmenting self- from allo-generated signals is crucial for active sensory processing. We report a dynamic filter used by South American pulse electric fish to distinguish active electro-sensory signals carried by their own electric discharges from other concomitant electrical stimuli (i.e. communication signals). The filter has a sensory component, consisting of an onset type central electro-sensory neuron, and a motor component, consisting of a change in the fish's discharge rate when allo-generated electrical events occur in temporal proximity to the fish's own discharge. We investigated the sensory component of the filter by in vitro mimicking synaptic inputs occurring during behavioral responses to allo-generated interfering signals. We found that active control of the discharge enhances self-generated over allo-generated responses by forcing allo-generated signals into a central refractory period. This hypothesis was confirmed by field potential recordings in freely discharging fish. Similar sensory-motor mechanisms may also contribute to signal segmentation in other sensory systems.

From the intrinsic properties to the functional role of a neuron phenotype: an example from electric fish during signal trade-off

“…Spherical neurons show a one-spike phenotype (Soares et al, 2002), as shown by whole-cell patch recordings in brain slices of the electrosensory lobe (Nogueria et al, 2006;Nogueira and Caputi, 2011) (Fig.1). This suggests the presence of a low-threshold, noninactivating K + conductance and a hyperpolarization-activated I h .…”

“…Four lines of argument support this affirmation (Nogueira et al, 2006;Nogueira and Caputi, 2011): (1) subthreshold pulses of increasing intensities are followed by a reduction of the depolarization caused by a second pulse (Fig.3A); (2) action potentials are followed by an increase in cell membrane conductance (Fig.3B) and an increase of spike threshold (Fig.3C) and (3) a long refractory period of similar time course (Fig.3D); and (4) this long refractory period is reduced under the treatment with low doses of the K + channel blocker 4AP (compare Fig.3D and 3E). …”

“…There is a persistent outward rectification dependent on a low-threshold K + conductance (K + LT ), and an inward rectification mediated by a mixed-cation conductance (I h ) (Wu and Oertel, 1984;Manis and Marx, 1991;Reyes et al, 1994;Brew and Forsythe, 1995;Rathouz and Trussell, 1998;Trussell, 1999;Golding et al, 1999;Oertel et al, 2000;Bal and Oertel, 2000;Soares et al, 2002;Koch and Grothe, 2003;MacLeod et al, 2006;Nogueira et al, 2006;Nogueira and Caputi, 2011).…”

“…Due to the one-spike onset response characteristic of the pulse markers and spherical neurons, the population activity evoked by the self-and allo-generated EODs can be recorded as a compound action potential at the nerve, ELL, lateral lemniscus and mesencephalic magnocellular nucleus (Castelló et al, 1998;Nogueira et al, 2006;Nogueira and Caputi, 2011) either in acute experiments or in chronically implanted freely moving fish. The changes in the self-generated local EOD introduced by the presence of objects modulate the firing latency of the pulse marker and spherical neuron axons.…”

“…The amplitude of the compound potential measured in the lateral lemniscus and in the nucleus magnocellularis is dependent on distance and position between fish (as it is expected by the change in the amplitude of the allo-generated electric image). Interestingly, even when both fish remain in a steady relative position, the stimulus-response relationship depends on the interval between the self-and allo-generated EODs (Fig.4) (Castelló et al, 1998;Nogueira et al, 2006;Nogueira and Caputi, 2011). Within a time window lasting approximately 5-10ms after the self-generated EOD, the axons of spherical neurons recorded in the lateral lemniscus and the neurons of the nucleus magnocellularis do not respond to further peripheral stimuli (Fig.4, frame 1, the artifact of the allogenerated EOD is marked as 'a').…”