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Clonal relationships impact neuronal tuning within a phylogenetically ancient vertebrate brain structure.

Muldal AM, Lillicrap TP, Richards BA, Akerman CJ - Curr. Biol. (2014)

Bottom Line: To address this question, we examined the influence of lineage on the response properties of neurons within the optic tectum, a visual brain area found in all vertebrates.If lineage relationships do not influence the functional properties of tectal neurons, one prediction is that the RF positions of sister neurons should be no more (or less) similar to one another than those of neighboring control neurons.Our data reveal that the RF centers of sister neurons are significantly more similar than would be expected by chance.

View Article: PubMed Central - PubMed

Affiliation: Department of Pharmacology, University of Oxford, Oxford OX1 3QT, UK.

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Sister Neurons in the Optic Tectum Have More Similar Spatial RFs Than Nonsisters(A) Relationship between spatial distance and Δcenter value for all pairs of tectal neurons (∗∗∗p < 0.001, ρ = 0.45, Spearman correlation). Inset illustrates how the Δcenter value was computed for a pair of RFs.(B) Δcenter values for sister and nonsister pairs of tectal neurons (data indicate mean ± SD; n = 13 clonal pairs and n = 72,546 nonclonal pairs from four animals in which a single clone was labeled; ∗∗∗p < 0.001, Mann-Whitney U test).(C) Spatial distances between somata of sister and nonsister pairs (∗∗∗p < 0.001, U test).(D) Schematic showing a pair of sister neurons and its corresponding set of spatially matched nonsister control pairs.(E) Cumulative distribution of Δcenter values for an example pair of sister neurons and its set of matched nonsister control pairs.(F) Pairwise bootstrap test confirms that sister neurons have more similar RF center positions than would be expected, given their spatial proximity within the tectum. Cyan distribution represents a random sample of mean percentile values (Supplemental Experimental Procedures). The mean percentile for sister pairs (red arrow) was significantly smaller than would be expected by chance (∗∗∗p < 0.001, bootstrap test).
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fig4: Sister Neurons in the Optic Tectum Have More Similar Spatial RFs Than Nonsisters(A) Relationship between spatial distance and Δcenter value for all pairs of tectal neurons (∗∗∗p < 0.001, ρ = 0.45, Spearman correlation). Inset illustrates how the Δcenter value was computed for a pair of RFs.(B) Δcenter values for sister and nonsister pairs of tectal neurons (data indicate mean ± SD; n = 13 clonal pairs and n = 72,546 nonclonal pairs from four animals in which a single clone was labeled; ∗∗∗p < 0.001, Mann-Whitney U test).(C) Spatial distances between somata of sister and nonsister pairs (∗∗∗p < 0.001, U test).(D) Schematic showing a pair of sister neurons and its corresponding set of spatially matched nonsister control pairs.(E) Cumulative distribution of Δcenter values for an example pair of sister neurons and its set of matched nonsister control pairs.(F) Pairwise bootstrap test confirms that sister neurons have more similar RF center positions than would be expected, given their spatial proximity within the tectum. Cyan distribution represents a random sample of mean percentile values (Supplemental Experimental Procedures). The mean percentile for sister pairs (red arrow) was significantly smaller than would be expected by chance (∗∗∗p < 0.001, bootstrap test).

Mentions: These data provided the opportunity to test whether clonal relationships influence the RF properties of tectal neurons. To quantify functional differences between pairs of tectal neurons, we computed the euclidean distance between the centers of their fitted RFs (Δcenter; Figure 4A). As expected, given the retinotopic organization of the tectum, there was a significant positive correlation between the spatial separation of pairs of neurons and their Δcenter values (Figure 4A). Although pairs of sister neurons had smaller Δcenter values than nonsister pairs (Figure 4B), they also tended to be situated closer to one another within the tectum (Figure 4C). Thus, to assess the effect of clonal relationships, it was crucial for us to control for the bias introduced by this spatial clustering. We therefore compared each pair of sister neurons with a spatially matched set of nonsister control pairs (Figure 4D; Supplemental Experimental Procedures). The spatially matched control pairs had to be situated in the same combination of tectal layers, and they had to be the same distance apart as the corresponding sister pairs, to within a tolerance of ±10 μm. We expressed the degree of functional similarity between each sister pair relative to its matched controls as a percentile (Figure 4E; Supplemental Experimental Procedures). Percentile values less than the median indicate neuron pairs that had more similar RF center positions than their average matched control pair. Across the population, we found that sister pairs had a significantly smaller average percentile value than would be expected by chance (p < 0.001, bootstrap test; Figures 4F and S1A; Supplemental Experimental Procedures). Thus, pairs of sister neurons show more similar RF center positions than would be expected, given their spatial proximity within the tectum. This bias was also evident when we excluded pairs of neurons located within the same tectal layer (Figure S1B).


Clonal relationships impact neuronal tuning within a phylogenetically ancient vertebrate brain structure.

Muldal AM, Lillicrap TP, Richards BA, Akerman CJ - Curr. Biol. (2014)

Sister Neurons in the Optic Tectum Have More Similar Spatial RFs Than Nonsisters(A) Relationship between spatial distance and Δcenter value for all pairs of tectal neurons (∗∗∗p < 0.001, ρ = 0.45, Spearman correlation). Inset illustrates how the Δcenter value was computed for a pair of RFs.(B) Δcenter values for sister and nonsister pairs of tectal neurons (data indicate mean ± SD; n = 13 clonal pairs and n = 72,546 nonclonal pairs from four animals in which a single clone was labeled; ∗∗∗p < 0.001, Mann-Whitney U test).(C) Spatial distances between somata of sister and nonsister pairs (∗∗∗p < 0.001, U test).(D) Schematic showing a pair of sister neurons and its corresponding set of spatially matched nonsister control pairs.(E) Cumulative distribution of Δcenter values for an example pair of sister neurons and its set of matched nonsister control pairs.(F) Pairwise bootstrap test confirms that sister neurons have more similar RF center positions than would be expected, given their spatial proximity within the tectum. Cyan distribution represents a random sample of mean percentile values (Supplemental Experimental Procedures). The mean percentile for sister pairs (red arrow) was significantly smaller than would be expected by chance (∗∗∗p < 0.001, bootstrap test).
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fig4: Sister Neurons in the Optic Tectum Have More Similar Spatial RFs Than Nonsisters(A) Relationship between spatial distance and Δcenter value for all pairs of tectal neurons (∗∗∗p < 0.001, ρ = 0.45, Spearman correlation). Inset illustrates how the Δcenter value was computed for a pair of RFs.(B) Δcenter values for sister and nonsister pairs of tectal neurons (data indicate mean ± SD; n = 13 clonal pairs and n = 72,546 nonclonal pairs from four animals in which a single clone was labeled; ∗∗∗p < 0.001, Mann-Whitney U test).(C) Spatial distances between somata of sister and nonsister pairs (∗∗∗p < 0.001, U test).(D) Schematic showing a pair of sister neurons and its corresponding set of spatially matched nonsister control pairs.(E) Cumulative distribution of Δcenter values for an example pair of sister neurons and its set of matched nonsister control pairs.(F) Pairwise bootstrap test confirms that sister neurons have more similar RF center positions than would be expected, given their spatial proximity within the tectum. Cyan distribution represents a random sample of mean percentile values (Supplemental Experimental Procedures). The mean percentile for sister pairs (red arrow) was significantly smaller than would be expected by chance (∗∗∗p < 0.001, bootstrap test).
Mentions: These data provided the opportunity to test whether clonal relationships influence the RF properties of tectal neurons. To quantify functional differences between pairs of tectal neurons, we computed the euclidean distance between the centers of their fitted RFs (Δcenter; Figure 4A). As expected, given the retinotopic organization of the tectum, there was a significant positive correlation between the spatial separation of pairs of neurons and their Δcenter values (Figure 4A). Although pairs of sister neurons had smaller Δcenter values than nonsister pairs (Figure 4B), they also tended to be situated closer to one another within the tectum (Figure 4C). Thus, to assess the effect of clonal relationships, it was crucial for us to control for the bias introduced by this spatial clustering. We therefore compared each pair of sister neurons with a spatially matched set of nonsister control pairs (Figure 4D; Supplemental Experimental Procedures). The spatially matched control pairs had to be situated in the same combination of tectal layers, and they had to be the same distance apart as the corresponding sister pairs, to within a tolerance of ±10 μm. We expressed the degree of functional similarity between each sister pair relative to its matched controls as a percentile (Figure 4E; Supplemental Experimental Procedures). Percentile values less than the median indicate neuron pairs that had more similar RF center positions than their average matched control pair. Across the population, we found that sister pairs had a significantly smaller average percentile value than would be expected by chance (p < 0.001, bootstrap test; Figures 4F and S1A; Supplemental Experimental Procedures). Thus, pairs of sister neurons show more similar RF center positions than would be expected, given their spatial proximity within the tectum. This bias was also evident when we excluded pairs of neurons located within the same tectal layer (Figure S1B).

Bottom Line: To address this question, we examined the influence of lineage on the response properties of neurons within the optic tectum, a visual brain area found in all vertebrates.If lineage relationships do not influence the functional properties of tectal neurons, one prediction is that the RF positions of sister neurons should be no more (or less) similar to one another than those of neighboring control neurons.Our data reveal that the RF centers of sister neurons are significantly more similar than would be expected by chance.

View Article: PubMed Central - PubMed

Affiliation: Department of Pharmacology, University of Oxford, Oxford OX1 3QT, UK.

Show MeSH
Related in: MedlinePlus