Sensory receptor diversity establishes a peripheral population code for stimulus duration at low intensities

Abstract

SUMMARY Peripheral filtering is a fundamental mechanism for establishing frequency tuning in sensory systems. By contrast, detection of temporal features, such as duration, is generally thought to result from temporal coding in the periphery, followed by an analysis of peripheral response times within the central nervous system. We investigated how peripheral filtering properties affect the coding of stimulus duration in the electrosensory system of mormyrid fishes using behavioral and electrophysiological measures of duration tuning. We recorded from individual knollenorgans, the electrosensory receptors that mediate communication, and found correlated variation in frequency tuning and duration tuning, as predicted by a simple circuit model. In response to relatively high intensity stimuli, knollenorgans responded reliably with fixed latency spikes, consistent with a temporal code for stimulus duration. At near-threshold intensities, however, both the reliability and the temporal precision of responses decreased. Evoked potential recordings from the midbrain, as well as behavioral responses to electrosensory stimulation, revealed changes in sensitivity across the range of durations associated with the greatest variability in receptor sensitivity. Further, this range overlapped with the natural range of variation in species-specific communication signals, suggesting that peripheral duration tuning affects the coding of behaviorally relevant stimuli. We measured knollenorgan, midbrain and behavioral responses to natural communication signals and found that each of them were duration dependent. We conclude that at relatively low intensities for which temporal coding is ineffective, diversity among sensory receptors establishes a population code, in which duration is reflected in the population of responding knollenorgans.

Multiplexed temporal coding of electric communication signals in mormyrid fishes

“…Variation in duration tuning among KOs may establish a population code for pulse duration at low intensities, when signaling fish are at a distance (Lyons-Warren et al, 2012a). At higher intensities, however, when signaling fish are close by and most of the receptors are responsive, a temporal code is used for encoding duration (Hopkins and Bass, 1981;Lyons-Warren et al, 2012a).…”

“…The canal is filled with a plug of loose epithelial cells, which adds a series capacitance to the organ (Zakon, 1986). This capacitance, along with the parallel resistive properties of the surrounding skin, makes the organ AC-coupled, establishing tuning to the high frequencies that characterize the power spectra of EODs (Bennett, 1965;Lyons-Warren et al, 2012a Fig.2. Neuroanatomy of the knollenorgan electrosensory (red), electromotor (blue) and corollary discharge (purple) pathways.…”

“…Variation in duration tuning among KOs may establish a population code for pulse duration at low intensities, when signaling fish are at a distance (Lyons-Warren et al, 2012a). At higher intensities, however, when signaling fish are close by and most of the receptors are responsive, a temporal code is used for encoding duration (Hopkins and Bass, 1981;Lyons-Warren et al, 2012a).KOs spike with a latency of ~100μs in response to positive changes in voltage across the skin, or inward current (Bennett, 1965). Because they are AC-coupled, KOs respond both to the onset of positive voltage steps and to the offset of negative voltage steps.…”

Detection of submillisecond spike timing differences based on delay-line anticoincidence detection

“…In response to an electrical stimulus, KOs on opposite sides of the body experience opposite stimulus polarities. Thus, in recordings from a single KO, the responses to normal and reversed polarity stimuli reveal how KOs on opposite sides of the body would respond to a single stimulus (Hopkins and Bass 1981;Lyons-Warren et al 2012). In the illustration, we show the spiking responses of a single KO, recorded extracellularly, to normal (simulating KO left ) and reversed (simulating KO right ) polarity square pulses of 2 different durations (left, 0.5 ms; right, 1 ms).…”

Differences in electrosensory anatomy and social behavior in an area of sympatry between two species of mormyrid electric fishes

“…Although the social behavior of petrocephalines has been less studied in the laboratory, petrocephaline species have been observed to school or shoal in captivity (Baker et al, 2015). In addition, the rosette knollenorgans of petrocephalines are maximally sensitive to the EOD interval patterns produced by these large groups (Baker et al, 2015), unlike the knollenorgan receptors of clade-A species, which are tuned to the power spectrum of the individual, species-specific EOD (Arnegard et al, 2006;Baker et al, 2015;Hopkins, 1981;Lyons-Warren et al, 2012). These various lines of evidence suggest that evolutionary divergence in the knollenorgan electrosensory pathway is related to differences in social behavior.…”