Processing Submillisecond Timing Differences in a Model Electrosensory System

Perception of sensory cues requires peripheral encoding followed by extraction of behaviorally relevant signal components by central neurons. Some sensory systems can detect temporal information with submillisecond accuracy, despite these signals occurring faster than the approximately 1 ms timescale of neuronal firing. In sound localization, the best studied example of this phenomenon, there are at least two distinct mechanisms for detecting submillisecond timing differences, indicating that multiple solutions to this fundamental problem exist. I investigated mechanisms for processing submillisecond timing differences by studying electrosensory processing in a time coding expert, mormyrid weakly electric fish, which can detect submillisecond differences in the duration of electric signals. First, I measured responses of peripheral receptors to stimuli of different durations. I found that each unit responded preferentially to longer stimuli, but with response thresholds that varied among units within the behaviorally relevant range of durations. This variability establishes a population code operating at near threshold intensities in which the number and identity of responding receptors represents duration. At higher stimulus intensities all units respond independent of duration, rendering the population code obsolete. Importantly, peripheral receptors respond either to the start or end of a signal. Thus, stimulus duration is also represented by a temporal code, as a difference in spike times between receptors. Next, I investigated the central mechanism for detection of submillisecond spike time differences by recording from time comparator neurons (Small Cells) in the midbrain. Recording from Small Cells is challenging because their somas are small and relatively inaccessible. I therefore designed a novel method using retrograde labeling to directly visualize and record from Small Cells in vivo. I showed that patterns of duration tuning vary among Small Cells due to a combination of blanking inhibition corresponding to one edge of a stimulus and variably delayed excitation corresponding to one or both edges of a stimulus. Other circuits that detect submillisecond timing differences rely either on precisely-timed inhibition or delay-line coincidence detection. I demonstrate a novel mechanism by which mormyrids combine delay-line coincidence detection with precisely-timed blanking inhibition to establish diverse patterns of duration tuning among a population of time comparators

Spatial stimulation of the electrosensory system of mormyrid electric fish

Spatial stimulation of the electrosensory system of mormyrid electric fis

Physiological evidence of sensory integration in the electrosensory lateral line lobe of Gnathonemus petersii

Fechner S, Grant K, von der Emde G, Engelmann J. Physiological evidence of sensory integration in the electrosensory lateral line lobe of Gnathonemus petersii. PLOS ONE. 2018;13(4): e0194347.Mormyrid fish rely on reafferent input for active electrolocation. Their electrosensory input consists of phase and amplitude information. These are encoded by differently tuned receptor cells within the Mormyromasts, A- and B-cells, respectively, which are distributed over the animal’s body. These convey their information to two topographically ordered medullary zones in the electrosensory lateral line lobe (ELL). The so-called medial zone receives only amplitude information, while the dorsolateral zone receives amplitude and phase information. Using both sources of information, Mormyrid fish can disambiguate electrical impedances. Where and how this disambiguation takes place is presently unclear. We here investigate phase-sensitivity downstream from the electroreceptors. We provide first evidence of phase-sensitivity in the medial zone of ELL. In this zone I-cells consistently decreased their rate to positive phase-shifts (6 of 20 cells) and increased their rate to negative shifts (11/20), while E-cells of the medial zone (3/9) responded oppositely to I-cells. In the dorsolateral zone the responses of E- and I-cells were opposite to those found in the medial zone. Tracer injections revealed interzonal projections that interconnect the dorsolateral and medial zones in a somatotopic manner. In summary, we show that phase information is processed differently in the dorsolateral and the medial zones. This is the first evidence for a mechanism that enhances the contrast between two parallel sensory channels in Mormyrid fish. This could be beneficial for impedance discrimination that ultimately must rely on a subtractive merging of these two sensory streams