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

View Article: PubMed Central - PubMed

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.

No MeSH data available.


Related in: MedlinePlus

Responses of LS pyramidal cells to chirps.A: Illustration of the methodology used to differentiate between the responses to the beat and to the chirp. The chirp stimuli of interest are shown in green and the corresponding responses from typical On-type (blue) and Off-type (red) neurons are also shown running the full extent of the stimulus. The response to a beat stimulus is then aligned in phase with the beat of the stimulus of interest both before and after the chirp. These two alignments are indicated by two separate dashed lines identified as the pre-chirp and post-chirp beat and run the full extent of the stimulus of interest. Directly beneath actual responses is a signal which can take on both positive and negative values as it was generated by subtracting the pre-chirp and post-chirp responses from the response to the stimulus of interest. The line running though or above this signal indicates a value of zero with positive values highlighted an appropriate color. The maximum value of this signal within the grey window (25 msec after chirp onset) is taken as the response of the neuron to the chirp. Responses to each of the four chirps are used to generate a 2 dimensional representation of the 4 dimensional response space known as a glyph. The correspondence between glyph dimensions and neural response to chirp phases are demonstrated for average On- and Off -type examples. Correspondence is indicated by highlighting the glyph axis associated with a given chirp phase on the glyph seen to the right of that chirp phase response. B: Peri-stimulus histograms from the same six example On-type cells used in Fig 2. Responses to the 4 different chirps were concatenated. Note that, while responses of superficial On-type cells to the beat are difficult to discern from the PSTH’s in Fig 2, their responses to chirps are quite clear. A glyph summarizing each example neuron’s location within the response space to these four chirps is located to the right of their PSTH and their logged peak firing rate response is indicated by a leftward or rightward pointing triangle on the adjacent colorbar. C: Same as in B but for 6 example Off-type neurons. D: Representation of the response space to 4 natural communication signals averaging over different populations. (Top left) Chirp responses of all On-type cells were averaged along each dimension of response space to generate an average “On glyph”. The same was done for all Off-type cells. Multidimensional scaling was used to project the response space into two dimensions and glyphs where plotted centered on their two coordinate representation. The visualization procedure was repeated but for more specific subpopulations by dividing On- and Off-type further into deep, intermediate, and superficial (bottom left). For comparison, the glyphs from individual neurons are also shown (right).
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pone.0175322.g006: Responses of LS pyramidal cells to chirps.A: Illustration of the methodology used to differentiate between the responses to the beat and to the chirp. The chirp stimuli of interest are shown in green and the corresponding responses from typical On-type (blue) and Off-type (red) neurons are also shown running the full extent of the stimulus. The response to a beat stimulus is then aligned in phase with the beat of the stimulus of interest both before and after the chirp. These two alignments are indicated by two separate dashed lines identified as the pre-chirp and post-chirp beat and run the full extent of the stimulus of interest. Directly beneath actual responses is a signal which can take on both positive and negative values as it was generated by subtracting the pre-chirp and post-chirp responses from the response to the stimulus of interest. The line running though or above this signal indicates a value of zero with positive values highlighted an appropriate color. The maximum value of this signal within the grey window (25 msec after chirp onset) is taken as the response of the neuron to the chirp. Responses to each of the four chirps are used to generate a 2 dimensional representation of the 4 dimensional response space known as a glyph. The correspondence between glyph dimensions and neural response to chirp phases are demonstrated for average On- and Off -type examples. Correspondence is indicated by highlighting the glyph axis associated with a given chirp phase on the glyph seen to the right of that chirp phase response. B: Peri-stimulus histograms from the same six example On-type cells used in Fig 2. Responses to the 4 different chirps were concatenated. Note that, while responses of superficial On-type cells to the beat are difficult to discern from the PSTH’s in Fig 2, their responses to chirps are quite clear. A glyph summarizing each example neuron’s location within the response space to these four chirps is located to the right of their PSTH and their logged peak firing rate response is indicated by a leftward or rightward pointing triangle on the adjacent colorbar. C: Same as in B but for 6 example Off-type neurons. D: Representation of the response space to 4 natural communication signals averaging over different populations. (Top left) Chirp responses of all On-type cells were averaged along each dimension of response space to generate an average “On glyph”. The same was done for all Off-type cells. Multidimensional scaling was used to project the response space into two dimensions and glyphs where plotted centered on their two coordinate representation. The visualization procedure was repeated but for more specific subpopulations by dividing On- and Off-type further into deep, intermediate, and superficial (bottom left). For comparison, the glyphs from individual neurons are also shown (right).

Mentions: Using this criterion, we found that our dataset was composed of 18 superficial, 15 intermediate and 4 deep On-type pyramidal cells and of 17 superficial, 14 intermediate, and 6 deep Off-type pyramidal cells. We then investigated how pyramidal cell heterogeneities influenced their responses to natural electro-communication “chirp” stimuli. To do so, we used four stimulus waveforms caused when a chirp occurs at different phases of the beat (Fig 6A, top panels, green). The responses of example On-type (blue) and Off-type (red) pyramidal cells to each chirp are shown in Fig 6A. Responses to all four chirps are then depicted as glyphs (Fig 6A).


Electrosensory neural responses to natural electro-communication stimuli are distributed along a continuum
Responses of LS pyramidal cells to chirps.A: Illustration of the methodology used to differentiate between the responses to the beat and to the chirp. The chirp stimuli of interest are shown in green and the corresponding responses from typical On-type (blue) and Off-type (red) neurons are also shown running the full extent of the stimulus. The response to a beat stimulus is then aligned in phase with the beat of the stimulus of interest both before and after the chirp. These two alignments are indicated by two separate dashed lines identified as the pre-chirp and post-chirp beat and run the full extent of the stimulus of interest. Directly beneath actual responses is a signal which can take on both positive and negative values as it was generated by subtracting the pre-chirp and post-chirp responses from the response to the stimulus of interest. The line running though or above this signal indicates a value of zero with positive values highlighted an appropriate color. The maximum value of this signal within the grey window (25 msec after chirp onset) is taken as the response of the neuron to the chirp. Responses to each of the four chirps are used to generate a 2 dimensional representation of the 4 dimensional response space known as a glyph. The correspondence between glyph dimensions and neural response to chirp phases are demonstrated for average On- and Off -type examples. Correspondence is indicated by highlighting the glyph axis associated with a given chirp phase on the glyph seen to the right of that chirp phase response. B: Peri-stimulus histograms from the same six example On-type cells used in Fig 2. Responses to the 4 different chirps were concatenated. Note that, while responses of superficial On-type cells to the beat are difficult to discern from the PSTH’s in Fig 2, their responses to chirps are quite clear. A glyph summarizing each example neuron’s location within the response space to these four chirps is located to the right of their PSTH and their logged peak firing rate response is indicated by a leftward or rightward pointing triangle on the adjacent colorbar. C: Same as in B but for 6 example Off-type neurons. D: Representation of the response space to 4 natural communication signals averaging over different populations. (Top left) Chirp responses of all On-type cells were averaged along each dimension of response space to generate an average “On glyph”. The same was done for all Off-type cells. Multidimensional scaling was used to project the response space into two dimensions and glyphs where plotted centered on their two coordinate representation. The visualization procedure was repeated but for more specific subpopulations by dividing On- and Off-type further into deep, intermediate, and superficial (bottom left). For comparison, the glyphs from individual neurons are also shown (right).
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pone.0175322.g006: Responses of LS pyramidal cells to chirps.A: Illustration of the methodology used to differentiate between the responses to the beat and to the chirp. The chirp stimuli of interest are shown in green and the corresponding responses from typical On-type (blue) and Off-type (red) neurons are also shown running the full extent of the stimulus. The response to a beat stimulus is then aligned in phase with the beat of the stimulus of interest both before and after the chirp. These two alignments are indicated by two separate dashed lines identified as the pre-chirp and post-chirp beat and run the full extent of the stimulus of interest. Directly beneath actual responses is a signal which can take on both positive and negative values as it was generated by subtracting the pre-chirp and post-chirp responses from the response to the stimulus of interest. The line running though or above this signal indicates a value of zero with positive values highlighted an appropriate color. The maximum value of this signal within the grey window (25 msec after chirp onset) is taken as the response of the neuron to the chirp. Responses to each of the four chirps are used to generate a 2 dimensional representation of the 4 dimensional response space known as a glyph. The correspondence between glyph dimensions and neural response to chirp phases are demonstrated for average On- and Off -type examples. Correspondence is indicated by highlighting the glyph axis associated with a given chirp phase on the glyph seen to the right of that chirp phase response. B: Peri-stimulus histograms from the same six example On-type cells used in Fig 2. Responses to the 4 different chirps were concatenated. Note that, while responses of superficial On-type cells to the beat are difficult to discern from the PSTH’s in Fig 2, their responses to chirps are quite clear. A glyph summarizing each example neuron’s location within the response space to these four chirps is located to the right of their PSTH and their logged peak firing rate response is indicated by a leftward or rightward pointing triangle on the adjacent colorbar. C: Same as in B but for 6 example Off-type neurons. D: Representation of the response space to 4 natural communication signals averaging over different populations. (Top left) Chirp responses of all On-type cells were averaged along each dimension of response space to generate an average “On glyph”. The same was done for all Off-type cells. Multidimensional scaling was used to project the response space into two dimensions and glyphs where plotted centered on their two coordinate representation. The visualization procedure was repeated but for more specific subpopulations by dividing On- and Off-type further into deep, intermediate, and superficial (bottom left). For comparison, the glyphs from individual neurons are also shown (right).
Mentions: Using this criterion, we found that our dataset was composed of 18 superficial, 15 intermediate and 4 deep On-type pyramidal cells and of 17 superficial, 14 intermediate, and 6 deep Off-type pyramidal cells. We then investigated how pyramidal cell heterogeneities influenced their responses to natural electro-communication “chirp” stimuli. To do so, we used four stimulus waveforms caused when a chirp occurs at different phases of the beat (Fig 6A, top panels, green). The responses of example On-type (blue) and Off-type (red) pyramidal cells to each chirp are shown in Fig 6A. Responses to all four chirps are then depicted as glyphs (Fig 6A).

View Article: PubMed Central - PubMed

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.

No MeSH data available.


Related in: MedlinePlus