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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.


A: At each step of the single linkage algorithm clusters are merged on the basis of the minimum distance between two observations each belonging to separate clusters. Which observations were linked at each iteration of the algorithm (nodes of the above dendrogram) and at what distance they were from each other within the original pairwise distance matrix was used to generate an adjacency matrix or network that was then represented as a network graph. At each two dimensional coordinate the glyph summarizing the observations location within the response space to 4 chirp stimuli was plotted and a colored letter indicating On- (blue) or Off-type (red), deep (D), intermediate (I) or superficial (S) was plotted atop this. B: Same as A but for DTW. C: Response profiles captured by 44 response features projected into a three dimensional feature space using an 8 Factor statistical model (χ2 = 1266 d.f. = 622 p = 3.47x10-46) accounted for 78% of the variance. Each observation is colored according to its anatomical designation and each observation is connected to the mean value of its anatomical class within the factor space. D: Network graph (desaturated black lines) constructed from an adjacency matrix where each observation was connected to the closest one half of the population using the warping distance between observations as entries with each mode labeled according to On- or Off-type as well as anatomical cell class. The mean coordinate for each of the six anatomical designations was computed and observations were linked to their respective groups mean.
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pone.0175322.g007: A: At each step of the single linkage algorithm clusters are merged on the basis of the minimum distance between two observations each belonging to separate clusters. Which observations were linked at each iteration of the algorithm (nodes of the above dendrogram) and at what distance they were from each other within the original pairwise distance matrix was used to generate an adjacency matrix or network that was then represented as a network graph. At each two dimensional coordinate the glyph summarizing the observations location within the response space to 4 chirp stimuli was plotted and a colored letter indicating On- (blue) or Off-type (red), deep (D), intermediate (I) or superficial (S) was plotted atop this. B: Same as A but for DTW. C: Response profiles captured by 44 response features projected into a three dimensional feature space using an 8 Factor statistical model (χ2 = 1266 d.f. = 622 p = 3.47x10-46) accounted for 78% of the variance. Each observation is colored according to its anatomical designation and each observation is connected to the mean value of its anatomical class within the factor space. D: Network graph (desaturated black lines) constructed from an adjacency matrix where each observation was connected to the closest one half of the population using the warping distance between observations as entries with each mode labeled according to On- or Off-type as well as anatomical cell class. The mean coordinate for each of the six anatomical designations was computed and observations were linked to their respective groups mean.

Mentions: Our results so far suggest that there is a relationship between function and anatomy in ELL pyramidal cells that is somewhat blurred by large overlap between the responses of the different anatomical cell classes. In order to further test this possibility, we retraced the steps of our single linkage clustering algorithm used after either CFA or DTW and the results are shown in Fig 7A and 7B, respectively. Inspection of these 2D network projections reveals that On-type neurons tend to be located at one end while Off-type neurons tend to be located at the other end (Fig 7A and 7B).


Electrosensory neural responses to natural electro-communication stimuli are distributed along a continuum
A: At each step of the single linkage algorithm clusters are merged on the basis of the minimum distance between two observations each belonging to separate clusters. Which observations were linked at each iteration of the algorithm (nodes of the above dendrogram) and at what distance they were from each other within the original pairwise distance matrix was used to generate an adjacency matrix or network that was then represented as a network graph. At each two dimensional coordinate the glyph summarizing the observations location within the response space to 4 chirp stimuli was plotted and a colored letter indicating On- (blue) or Off-type (red), deep (D), intermediate (I) or superficial (S) was plotted atop this. B: Same as A but for DTW. C: Response profiles captured by 44 response features projected into a three dimensional feature space using an 8 Factor statistical model (χ2 = 1266 d.f. = 622 p = 3.47x10-46) accounted for 78% of the variance. Each observation is colored according to its anatomical designation and each observation is connected to the mean value of its anatomical class within the factor space. D: Network graph (desaturated black lines) constructed from an adjacency matrix where each observation was connected to the closest one half of the population using the warping distance between observations as entries with each mode labeled according to On- or Off-type as well as anatomical cell class. The mean coordinate for each of the six anatomical designations was computed and observations were linked to their respective groups mean.
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC5383285&req=5

pone.0175322.g007: A: At each step of the single linkage algorithm clusters are merged on the basis of the minimum distance between two observations each belonging to separate clusters. Which observations were linked at each iteration of the algorithm (nodes of the above dendrogram) and at what distance they were from each other within the original pairwise distance matrix was used to generate an adjacency matrix or network that was then represented as a network graph. At each two dimensional coordinate the glyph summarizing the observations location within the response space to 4 chirp stimuli was plotted and a colored letter indicating On- (blue) or Off-type (red), deep (D), intermediate (I) or superficial (S) was plotted atop this. B: Same as A but for DTW. C: Response profiles captured by 44 response features projected into a three dimensional feature space using an 8 Factor statistical model (χ2 = 1266 d.f. = 622 p = 3.47x10-46) accounted for 78% of the variance. Each observation is colored according to its anatomical designation and each observation is connected to the mean value of its anatomical class within the factor space. D: Network graph (desaturated black lines) constructed from an adjacency matrix where each observation was connected to the closest one half of the population using the warping distance between observations as entries with each mode labeled according to On- or Off-type as well as anatomical cell class. The mean coordinate for each of the six anatomical designations was computed and observations were linked to their respective groups mean.
Mentions: Our results so far suggest that there is a relationship between function and anatomy in ELL pyramidal cells that is somewhat blurred by large overlap between the responses of the different anatomical cell classes. In order to further test this possibility, we retraced the steps of our single linkage clustering algorithm used after either CFA or DTW and the results are shown in Fig 7A and 7B, respectively. Inspection of these 2D network projections reveals that On-type neurons tend to be located at one end while Off-type neurons tend to be located at the other end (Fig 7A and 7B).

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.