Weakly electric fish give behavioral responses to envelopes naturally occurring during movement: implications for neural processing

Abstract

How the brain processes natural sensory input remains an important and poorly understood problem in neuroscience. The efficient coding hypothesis asserts that the brain's coding strategies are adapted to the statistics of natural stimuli in order to efficiently process them, thereby optimizing their perception by the organism. Here we examined whether gymnotiform weakly electric fish displayed behavioral responses that are adapted to the statistics of the natural electrosensory envelopes. Previous studies have shown that the envelopes resulting from movement tend to consist of low (<1 Hz) temporal frequencies and are behaviorally relevant whereas those resulting from social interactions consist of higher (>1 Hz) temporal frequencies that can thus mask more behaviorally relevant signals. We found that the self-generated electric organ discharge frequency follows the detailed time course of the envelope around a mean value that is positively offset with respect to its baseline value for temporal frequencies between 0.001 Hz and 1 Hz. The frequency-following component of this behavioral response decreased in magnitude as a power law as a function of the envelope frequency and was negligible for envelope frequencies above 1 Hz. In contrast, the offset component was relatively constant and somewhat increased for envelope frequencies above 1 Hz. Thus, our results show that weakly electric fish display behavioral responses that track the detailed time course of low but not high frequency envelope stimuli. Furthermore, we found that the magnitude of the frequency-following behavioral response matches, in a one-to-one fashion, the spectral power of natural second-order stimulus attributes observed during movement. Indeed, both decayed as a power law with the same exponent for temporal frequencies spanning three orders of magnitude. Thus, our findings suggest that the neural coding strategies used by weakly electric fish perceive the detailed time course of movement envelopes and are adapted to their statistics as found in the natural environment. They also suggest that weakly electric fish might take advantage of the differential frequency content of movement and social envelopes in order to give appropriate behavioral responses during encounters between two or more conspecifics.

Electrosensory processing inApteronotus albifrons: implications for general and specific neural coding strategies across wave-type weakly electric fish species

“…Thus our results provide strong support for the hypothesis that both species use nearly identical strategies for processing envelopes. While further studies are needed to investigate the statistics of natural envelope stimuli in A. albifrons, we predict that these should be very similar if not identical to those observed for A. leptorhynchus (Fotowat et al 2013;Metzen and Chacron 2014;Yu et al 2012). We further predict that the fractional differentiation exponent seen in A. albifrons should be matched to natural envelope statistics, such that ELL pyramidal cells optimally encode envelopes through temporal whitening, as observed for A. leptorhynchus .…”

“…We chose these particular frequency bands because they have been used It is important to note here that all AM stimuli described so far consisted of only first order time varying features. However, natural electrosensory stimuli are characterized by both first and second order features (Fotowat et al 2013;Metzen and Chacron 2014;Stamper et al 2013). In particular, movement will cause changes in the beat amplitude when two fish interact.…”

Coding of envelopes by correlated but not single-neuron activity requires neural variability

“…Response nonlinearities (e.g., rectification, phase-locking) are more likely to be elicited by stimuli with relatively large intensities (40)(41)(42). However, natural stimuli are usually characterized by relatively low intensities yet can give rise to robust behavioral responses (13,17,43,44). In these conditions, our results show that single-neuron activity instead does not provide detailed information about the envelope.…”

“…In the electrosensory system, second-order attributes carry important information about the relative distance between conspecifics (11). It is likely that higher brain areas decode information about second-order attributes carried by correlated electroreceptor activity because weakly electric fish display strong and reliable behavioral responses to these attributes (13). Indeed, pyramidal cells within the electrosensory lateral line lobe strongly respond to envelopes at the single-neuron level (36) presumably through nonlinear integration of afferent synaptic input (26).…”

“…Peripheral electroreceptor afferents scattered over the animal's skin respond to the low-intensity changes in EOD amplitude frequently encountered under natural conditions (11) through linearly related changes in firing rate (12). Although previous studies have shown that envelope information under these conditions reaches higher brain regions, thus giving rise to perception and behavior (13), the processing of low-intensity envelopes by the afferent population is not well understood.…”