Electrosensory neural responses to natural electro-communication stimuli are distributed along a continuum

Abstract

Neural heterogeneities are seen ubiquitously within the brain and greatly complicate classification efforts. Here we tested whether the responses of an anatomically well-characterized sensory neuron population to natural stimuli could be used for functional classification. To do so, we recorded from pyramidal cells within the electrosensory lateral line lobe (ELL) of the weakly electric fish Apteronotus leptorhynchus in response to natural electro-communication stimuli as these cells can be anatomically classified into six different types. We then used two independent methodologies to functionally classify responses: one relies of reducing the dimensionality of a feature space while the other directly compares the responses themselves. Both methodologies gave rise to qualitatively similar results: while ON and OFF-type cells could easily be distinguished from one another, ELL pyramidal neuron responses are actually distributed along a continuum rather than forming distinct clusters due to heterogeneities. We discuss the implications of our results for neural coding and highlight some potential advantages.

Synergistic population coding of natural communication stimuli by hindbrain electrosensory neurons

“…We waited at least one hour after probe insertion before starting recordings to allow brain tissue to settle following probe insertion and to improve recording stability. Accounting for the fact that the first recording site is located 175 μm away from the tip along the probe shaft, as well as the fact that recordings were typically obtained on recording sites ranging between 13 and 97, this gives approximate recording between 355 and 1195 μm from the brain surface along, which are within the range reported from a previous study where location within LS was confirmed by histological post-processing 82 , 83 . Thus, based on probe geometry, anatomy 81 , and our experience recording from ELL pyramidal cells 58 , 65 , 82 , 84 , 85 , it is likely that most of our recordings were from LS.…”

Neural Network Organization for Courtship Song Feature Detection inDrosophila

“…These results rule out a model in which the two main song modes are processed in separate pathways, and instead support a model in which interconnectivity contributes to generating a continuum of song mode preferences. Such a continuum has been observed in the sensory systems of fish (Sproule and Chacron, 2017; Thompson and Scott, 2016) and sensorimotor cortices of rodents ((Minderer et al, 2019); (Raposo et al, 2014); (Saleem et al, 2013)), and thought to support encoding of a larger array of variables than would be possible with categorical representations (in other words, a more efficient representation). In the fly auditory system, neurons with intermediate preference could encode sound intensity, location, and long timescale features, such as the variable sequence of pulses and sines that make up song bouts (Coen et al, 2014) - behavioral studies demonstrate that females are sensitive to song bout features such as the average duration of song bouts over timescales of minutes (Clemens et al, 2015).…”

Neural network organization for courtship-song feature detection in Drosophila

“…We tested this by predicting responses at each node in the connectome from the responses of the inputs using a simple linear model (Figure 6) and discovered strong predictability, suggesting that the wiring diagram places a strong constraint on functional responses, consistent with recent studies in the fly olfactory system. 50 Response continuums have been observed in fish 51,52 and rodents, [53][54][55] and are thought to support more efficient encoding than would be possible with categorical representations. In the fly auditory system, neurons with intermediate preference (that respond roughly equally to sine and pulse) could encode sound intensity, location, and/or long timescale features, such as the variable sequence of pulses and sines that make up song bouts.…”