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Genetic control of startle behavior in medaka fish.

Tsuboko S, Kimura T, Shinya M, Suehiro Y, Okuyama T, Shimada A, Takeda H, Naruse K, Kubo T, Takeuchi H - PLoS ONE (2014)

Bottom Line: Our findings suggested behavioral diversity of the startle response within a local population as well as among different populations.Our findings are the first to suggest that a single genomic region might be sufficient to generate individual differences in startle behavior between wild-type strains.Further identification of genetic polymorphisms that define the behavioral trait will contribute to our understanding of the neural mechanisms underlying behavioral diversity, allowing us to investigate the adaptive significance of intraspecific behavioral polymorphisms of the startle response.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo, Tokyo, Japan.

ABSTRACT
Genetic polymorphisms are thought to generate intraspecific behavioral diversities, both within and among populations. The mechanisms underlying genetic control of behavioral properties, however, remain unclear in wild-type vertebrates, including humans. To explore this issue, we used diverse inbred strains of medaka fish (Oryzias latipes) established from the same and different local populations. Medaka exhibit a startle response to a visual stimulus (extinction of illumination) by rapidly bending their bodies (C-start) 20-ms after the stimulus presentation. We measured the rates of the response to repeated stimuli (1-s interval, 40 times) among four inbred strains, HNI-I, HNI-II, HO5, and Hd-rR-II1, and quantified two properties of the startle response: sensitivity (response rate to the first stimulus) and attenuation of the response probability with repeated stimulus presentation. Among the four strains, the greatest differences in these properties were detected between HNI-II and Hd-rR-II1. HNI-II exhibited high sensitivity (approximately 80%) and no attenuation, while Hd-rR-II1 exhibited low sensitivity (approximately 50%) and almost complete attenuation after only five stimulus presentations. Our findings suggested behavioral diversity of the startle response within a local population as well as among different populations. Linkage analysis with F2 progeny between HNI-II and Hd-rR-II1 detected quantitative trait loci (QTL) highly related to attenuation, but not to sensitivity, with a maximum logarithm of odds score of 11.82 on linkage group 16. The three genotypes (homozygous for HNI-II and Hd-rR-II1 alleles, and heterozygous) at the marker nearest the QTL correlated with attenuation. Our findings are the first to suggest that a single genomic region might be sufficient to generate individual differences in startle behavior between wild-type strains. Further identification of genetic polymorphisms that define the behavioral trait will contribute to our understanding of the neural mechanisms underlying behavioral diversity, allowing us to investigate the adaptive significance of intraspecific behavioral polymorphisms of the startle response.

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Comparison of Startle Response Properties among Inbred Strains.HNI-II (n = 20), HNI-I (n = 6), HO5 (n = 14), Hd-rR-II1 (n = 20). (A) Transition of response probability. Bars represent SEM. (B) Sensitivity of four inbred strains. Bars represent SEM. ** p<0.01 by Scheffe's F test. (C) Response stability index of four inbred strains. Bars represent SEM. a, b, c, d, and e indicate p<0.01 by Scheffe's F test.
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pone-0112527-g002: Comparison of Startle Response Properties among Inbred Strains.HNI-II (n = 20), HNI-I (n = 6), HO5 (n = 14), Hd-rR-II1 (n = 20). (A) Transition of response probability. Bars represent SEM. (B) Sensitivity of four inbred strains. Bars represent SEM. ** p<0.01 by Scheffe's F test. (C) Response stability index of four inbred strains. Bars represent SEM. a, b, c, d, and e indicate p<0.01 by Scheffe's F test.

Mentions: To investigate changes in the startle response to repeated eliciting stimuli, we used blinking stimuli, where the entire screen flickered 40 times at 1-s intervals (Figure 1B). We examined whether fish exhibited the startle response to each eliciting stimulus based on recorded movies (Figure 1A and 1C). This behavioral test was performed in the same fish everyday for five consecutive days and the startle response rate of each fish was calculated for every stimulus (Figure 2A). Among the four strains, the most prominent differences were detected between HNI-II and Hd-rR-II1 in two features, although neither strain exhibited a significantly decreased maximum velocity during the response (i.e. response magnitude) and both continued to respond (one-way ANOVA; HNI-II: F (39, 685)  = 1.14, p>0.05; Hd-rR-II1: F (3, 28)  = 2.11, p>0.05; Figure S1A). HNI-II demonstrated the highest sensitivity and no attenuation of response probability, and Hd-rR-II1 demonstrated the lowest sensitivity and almost complete attenuation of response probability within five repeated stimulus presentations. To quantitatively compare the response properties, we defined two indexes. The “sensitivity index” was defined as the probability of a response to the first eliciting stimulus on each of the 5 days. The “response stability index” was defined as the number of eliciting stimuli needed before an integrated response reached half the total amount (see Materials and Methods), which negatively correlates with the degree of attenuation. No effect of day on either of the indices was detected (two-way repeated measures ANOVA; sensitivity: F (4, 280)  = 0.31, p>0.05; response stability index: F (4, 280)  = 1.03, p>0.05; Figure S2). The sensitivity index was significantly different between HNI-II and Hd-rR-II1 (Scheffe's F test, p<0.01; Figure 2B and S3A) among the four inbred strain, while the response stability index was significantly different among several combinations (Figure 2C and S3B). HNI-I and HNI-II both originated from the same local-wild population or a “deme” (Niigata stock), belonging to the Northern Japan population [13], [14], [20], while Hd-rR-II1 and HO5 originated from different stocks in the Southern Japan population [13], [14], [20].


Genetic control of startle behavior in medaka fish.

Tsuboko S, Kimura T, Shinya M, Suehiro Y, Okuyama T, Shimada A, Takeda H, Naruse K, Kubo T, Takeuchi H - PLoS ONE (2014)

Comparison of Startle Response Properties among Inbred Strains.HNI-II (n = 20), HNI-I (n = 6), HO5 (n = 14), Hd-rR-II1 (n = 20). (A) Transition of response probability. Bars represent SEM. (B) Sensitivity of four inbred strains. Bars represent SEM. ** p<0.01 by Scheffe's F test. (C) Response stability index of four inbred strains. Bars represent SEM. a, b, c, d, and e indicate p<0.01 by Scheffe's F test.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4231031&req=5

pone-0112527-g002: Comparison of Startle Response Properties among Inbred Strains.HNI-II (n = 20), HNI-I (n = 6), HO5 (n = 14), Hd-rR-II1 (n = 20). (A) Transition of response probability. Bars represent SEM. (B) Sensitivity of four inbred strains. Bars represent SEM. ** p<0.01 by Scheffe's F test. (C) Response stability index of four inbred strains. Bars represent SEM. a, b, c, d, and e indicate p<0.01 by Scheffe's F test.
Mentions: To investigate changes in the startle response to repeated eliciting stimuli, we used blinking stimuli, where the entire screen flickered 40 times at 1-s intervals (Figure 1B). We examined whether fish exhibited the startle response to each eliciting stimulus based on recorded movies (Figure 1A and 1C). This behavioral test was performed in the same fish everyday for five consecutive days and the startle response rate of each fish was calculated for every stimulus (Figure 2A). Among the four strains, the most prominent differences were detected between HNI-II and Hd-rR-II1 in two features, although neither strain exhibited a significantly decreased maximum velocity during the response (i.e. response magnitude) and both continued to respond (one-way ANOVA; HNI-II: F (39, 685)  = 1.14, p>0.05; Hd-rR-II1: F (3, 28)  = 2.11, p>0.05; Figure S1A). HNI-II demonstrated the highest sensitivity and no attenuation of response probability, and Hd-rR-II1 demonstrated the lowest sensitivity and almost complete attenuation of response probability within five repeated stimulus presentations. To quantitatively compare the response properties, we defined two indexes. The “sensitivity index” was defined as the probability of a response to the first eliciting stimulus on each of the 5 days. The “response stability index” was defined as the number of eliciting stimuli needed before an integrated response reached half the total amount (see Materials and Methods), which negatively correlates with the degree of attenuation. No effect of day on either of the indices was detected (two-way repeated measures ANOVA; sensitivity: F (4, 280)  = 0.31, p>0.05; response stability index: F (4, 280)  = 1.03, p>0.05; Figure S2). The sensitivity index was significantly different between HNI-II and Hd-rR-II1 (Scheffe's F test, p<0.01; Figure 2B and S3A) among the four inbred strain, while the response stability index was significantly different among several combinations (Figure 2C and S3B). HNI-I and HNI-II both originated from the same local-wild population or a “deme” (Niigata stock), belonging to the Northern Japan population [13], [14], [20], while Hd-rR-II1 and HO5 originated from different stocks in the Southern Japan population [13], [14], [20].

Bottom Line: Our findings suggested behavioral diversity of the startle response within a local population as well as among different populations.Our findings are the first to suggest that a single genomic region might be sufficient to generate individual differences in startle behavior between wild-type strains.Further identification of genetic polymorphisms that define the behavioral trait will contribute to our understanding of the neural mechanisms underlying behavioral diversity, allowing us to investigate the adaptive significance of intraspecific behavioral polymorphisms of the startle response.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo, Tokyo, Japan.

ABSTRACT
Genetic polymorphisms are thought to generate intraspecific behavioral diversities, both within and among populations. The mechanisms underlying genetic control of behavioral properties, however, remain unclear in wild-type vertebrates, including humans. To explore this issue, we used diverse inbred strains of medaka fish (Oryzias latipes) established from the same and different local populations. Medaka exhibit a startle response to a visual stimulus (extinction of illumination) by rapidly bending their bodies (C-start) 20-ms after the stimulus presentation. We measured the rates of the response to repeated stimuli (1-s interval, 40 times) among four inbred strains, HNI-I, HNI-II, HO5, and Hd-rR-II1, and quantified two properties of the startle response: sensitivity (response rate to the first stimulus) and attenuation of the response probability with repeated stimulus presentation. Among the four strains, the greatest differences in these properties were detected between HNI-II and Hd-rR-II1. HNI-II exhibited high sensitivity (approximately 80%) and no attenuation, while Hd-rR-II1 exhibited low sensitivity (approximately 50%) and almost complete attenuation after only five stimulus presentations. Our findings suggested behavioral diversity of the startle response within a local population as well as among different populations. Linkage analysis with F2 progeny between HNI-II and Hd-rR-II1 detected quantitative trait loci (QTL) highly related to attenuation, but not to sensitivity, with a maximum logarithm of odds score of 11.82 on linkage group 16. The three genotypes (homozygous for HNI-II and Hd-rR-II1 alleles, and heterozygous) at the marker nearest the QTL correlated with attenuation. Our findings are the first to suggest that a single genomic region might be sufficient to generate individual differences in startle behavior between wild-type strains. Further identification of genetic polymorphisms that define the behavioral trait will contribute to our understanding of the neural mechanisms underlying behavioral diversity, allowing us to investigate the adaptive significance of intraspecific behavioral polymorphisms of the startle response.

Show MeSH
Related in: MedlinePlus