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Statistical significance of precisely repeated intracellular synaptic patterns.

Ikegaya Y, Matsumoto W, Chiou HY, Yuste R, Aaron G - PLoS ONE (2008)

Bottom Line: To test this hypothesis, we devised a method for finding precise repeats of activity and compared repeats found in the data to those found in surrogate datasets made by shuffling the original data.Our reanalysis reveals that repeats are statistically significant, thus supporting our earlier conclusions, while also supporting many conclusions that Mokeichev et al. (2007) drew from their recent in vivo recordings.In conclusion, our reevaluation resolves the methodological contradictions between Ikegaya et al. (2004) and Mokeichev et al. (2007), but demonstrates the validity of our previous conclusion that spontaneous network activity is non-randomly organized.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo, Japan.

ABSTRACT
Can neuronal networks produce patterns of activity with millisecond accuracy? It may seem unlikely, considering the probabilistic nature of synaptic transmission. However, some theories of brain function predict that such precision is feasible and can emerge from the non-linearity of the action potential generation in circuits of connected neurons. Several studies have presented evidence for and against this hypothesis. Our earlier work supported the precision hypothesis, based on results demonstrating that precise patterns of synaptic inputs could be found in intracellular recordings from neurons in brain slices and in vivo. To test this hypothesis, we devised a method for finding precise repeats of activity and compared repeats found in the data to those found in surrogate datasets made by shuffling the original data. Because more repeats were found in the original data than in the surrogate data sets, we argued that repeats were not due to chance occurrence. Mokeichev et al. (2007) challenged these conclusions, arguing that the generation of surrogate data was insufficiently rigorous. We have now reanalyzed our previous data with the methods introduced from Mokeichev et al. (2007). Our reanalysis reveals that repeats are statistically significant, thus supporting our earlier conclusions, while also supporting many conclusions that Mokeichev et al. (2007) drew from their recent in vivo recordings. Moreover, we also show that the conditions under which the membrane potential is recorded contributes significantly to the ability to detect repeats and may explain conflicting results. In conclusion, our reevaluation resolves the methodological contradictions between Ikegaya et al. (2004) and Mokeichev et al. (2007), but demonstrates the validity of our previous conclusion that spontaneous network activity is non-randomly organized.

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Three examples of repeats found using the PHRI detector from a 190 second long cat in vivo current clamp recording.Each motif-repeat example is labeled with its respective PHRI and its length. The PHRI values are a subset of those that make up the full set of PHRI values for this recording that are displayed in Fig. 8c.
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pone-0003983-g009: Three examples of repeats found using the PHRI detector from a 190 second long cat in vivo current clamp recording.Each motif-repeat example is labeled with its respective PHRI and its length. The PHRI values are a subset of those that make up the full set of PHRI values for this recording that are displayed in Fig. 8c.

Mentions: We then used the PHRI analysis with the original 190 second recording, computing PHRI values from the original and fifty 400 msec interval shuffled surrogates. The rank ordered distributions of these scores are normally distributed for each rank order (using Jarque-Bera test of normality), allowing confidence intervals to be computed. As shown, the distribution of the PHRI scores for the original recording is outside the 99% confidence interval computed from the 50 shuffled surrogates (Fig. 8C). Motif-repeat examples from the original recording, selected from a range of PHRI values, are displayed in Figure 9.


Statistical significance of precisely repeated intracellular synaptic patterns.

Ikegaya Y, Matsumoto W, Chiou HY, Yuste R, Aaron G - PLoS ONE (2008)

Three examples of repeats found using the PHRI detector from a 190 second long cat in vivo current clamp recording.Each motif-repeat example is labeled with its respective PHRI and its length. The PHRI values are a subset of those that make up the full set of PHRI values for this recording that are displayed in Fig. 8c.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2599887&req=5

pone-0003983-g009: Three examples of repeats found using the PHRI detector from a 190 second long cat in vivo current clamp recording.Each motif-repeat example is labeled with its respective PHRI and its length. The PHRI values are a subset of those that make up the full set of PHRI values for this recording that are displayed in Fig. 8c.
Mentions: We then used the PHRI analysis with the original 190 second recording, computing PHRI values from the original and fifty 400 msec interval shuffled surrogates. The rank ordered distributions of these scores are normally distributed for each rank order (using Jarque-Bera test of normality), allowing confidence intervals to be computed. As shown, the distribution of the PHRI scores for the original recording is outside the 99% confidence interval computed from the 50 shuffled surrogates (Fig. 8C). Motif-repeat examples from the original recording, selected from a range of PHRI values, are displayed in Figure 9.

Bottom Line: To test this hypothesis, we devised a method for finding precise repeats of activity and compared repeats found in the data to those found in surrogate datasets made by shuffling the original data.Our reanalysis reveals that repeats are statistically significant, thus supporting our earlier conclusions, while also supporting many conclusions that Mokeichev et al. (2007) drew from their recent in vivo recordings.In conclusion, our reevaluation resolves the methodological contradictions between Ikegaya et al. (2004) and Mokeichev et al. (2007), but demonstrates the validity of our previous conclusion that spontaneous network activity is non-randomly organized.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Chemical Pharmacology, Graduate School of Pharmaceutical Sciences, The University of Tokyo, Tokyo, Japan.

ABSTRACT
Can neuronal networks produce patterns of activity with millisecond accuracy? It may seem unlikely, considering the probabilistic nature of synaptic transmission. However, some theories of brain function predict that such precision is feasible and can emerge from the non-linearity of the action potential generation in circuits of connected neurons. Several studies have presented evidence for and against this hypothesis. Our earlier work supported the precision hypothesis, based on results demonstrating that precise patterns of synaptic inputs could be found in intracellular recordings from neurons in brain slices and in vivo. To test this hypothesis, we devised a method for finding precise repeats of activity and compared repeats found in the data to those found in surrogate datasets made by shuffling the original data. Because more repeats were found in the original data than in the surrogate data sets, we argued that repeats were not due to chance occurrence. Mokeichev et al. (2007) challenged these conclusions, arguing that the generation of surrogate data was insufficiently rigorous. We have now reanalyzed our previous data with the methods introduced from Mokeichev et al. (2007). Our reanalysis reveals that repeats are statistically significant, thus supporting our earlier conclusions, while also supporting many conclusions that Mokeichev et al. (2007) drew from their recent in vivo recordings. Moreover, we also show that the conditions under which the membrane potential is recorded contributes significantly to the ability to detect repeats and may explain conflicting results. In conclusion, our reevaluation resolves the methodological contradictions between Ikegaya et al. (2004) and Mokeichev et al. (2007), but demonstrates the validity of our previous conclusion that spontaneous network activity is non-randomly organized.

Show MeSH
Related in: MedlinePlus