Monthly Archives: March 2017

How to compare dependent correlations

In this post we’re going to compare two robust dependent correlation coefficients using a frequentist approach. The approach boils down to computing a confidence interval for the difference between correlations. There are several solutions to this problem, and we’re going to focus on what is probably the simplest one, using a percentile bootstrap, as described in Wilcox 2016 & implemented in his R functions twoDcorR() and twoDNOV(). These two functions correspond to two cases:

  • Case 1: overlapping correlations
  • Case 2: non-overlapping correlations

Case 1: overlapping correlations

Case 1 corresponds to the common scenario in which we look for correlations, across participants, between one behavioural measurement and activity in several brain areas. For instance, we could look at correlations between percent correct in one task and brain activity in two regions of interest (e.g. parietal and occipital). In this scenario, often papers report a significant brain-behaviour correlation in one brain area, and a non-significant correlation in another brain area. Stopping the analyses at that stage leads to a common interaction fallacy: because correlation 1 is statistically significant and correlation 2 is not does not mean that the two correlations differ (Nieuwenhuis et al. 2011). The interaction fallacy is also covered in a post by Jan Vanhove. Thom Baguley also provides R code to compare correlations, as well as a cautionary note about using correlations at all.

To compare the two correlation coefficients, we proceed like this:

  • sample participants with replacement
  • compute the two correlation coefficients based on the bootstrap samples
  • save the difference between correlations
  • execute the previous steps at least 500 times
  • use the distribution of bootstrap differences to derive a confidence interval: a 95% confidence interval is defined as the 2.5th and 97.5th quantiles of the bootstrap distribution.

A Matlab script implementing the procedure is on github. To run the code you will need the Robust Correlation Toolbox. First we generate data and illustrate them.

fig1_comp2dcorr

Figure 1

% Then we bootstrap the data
Nb = 500;
bootcorr1 = zeros(Nb,1);
bootcorr2 = zeros(Nb,1);

for B = 1:Nb

bootsample = randi(Np,1,Np);
bootcorr1(B) = Spearman(a(bootsample),b(bootsample),0);
bootcorr2(B) = Spearman(a(bootsample),c(bootsample),0);

end

% Cyril Pernet pointed out on Twitter that the loop is unnecessary.
% We can compute all bootstrap samples in one go:
% bootsamples = randi(Np,Np,Nb);
% bc1 = Spearman(a(bootsamples),b(bootsamples),0);
% bc2 = Spearman(a(bootsamples),c(bootsamples),0);
% The bootstrap loop does make the bootstrap procedure more intuitive
% for new users, especially if they are also learning R or Matlab!

In the example above we used Spearman’s correlation, which is robust to univariate outliers (Pernet, Wilcox & Rousselet, 2012). To apply the technique to Pearson’s correlation, the boundaries of the confidence interval need to be adjusted, as described in Wilcox (2009). However, Pearson’s correlation is not robust so it should be used cautiously (Rousselet & Pernet 2012). Also, as described in Wilcox (2009), Fisher’s z test to compare correlation coefficients is inappropriate.

Confidence intervals are obtained like this:

alpha = 0.05; % probability coverage - 0.05 for 95% CI

hi = floor((1-alpha/2)*Nb+.5);
lo = floor((alpha/2)*Nb+.5);

% for each correlation
boot1sort = sort(bootcorr1);
boot2sort = sort(bootcorr2);
boot1ci = [boot1sort(lo) boot1sort(hi)]; 
boot2ci = [boot2sort(lo) boot2sort(hi)]; 

% for the difference between correlations
bootdiff = bootcorr1 - bootcorr2;
bootdiffsort = sort(bootdiff);
diffci = [bootdiffsort(lo) bootdiffsort(hi)];

We get:

corr(a,b) = 0.52 [0.34 0.66]
corr(a,c) = 0.79 [0.68 0.86]
difference = -0.27 [-0.44 -0.14]

The bootstrap distribution of the differences between correlation coefficients is illustrated below.

fig2_comp2dcorr

Figure 2

The bootstrap distribution does not overlap with zero, our null hypothesis. In that case the p value is exactly zero, which is calculated like this:

pvalue = mean(bootdiffsort < 0);
pvalue = 2*min(pvalue,1-pvalue);

The original difference between coefficients is marked by a thick vertical black line. The 95% percentile bootstrap confidence interval is illustrated by the two thin vertical black lines.

Case 2: non-overlapping correlations

Case 2 corresponds to a before-after scenario. For instance the same participants are tested before and after an intervention, such as a training procedure. On each occasion, we compute a correlation, say between brain activity and behaviour, and we want to know if that correlation changes following the intervention.

This case 2 is addressed using a straightforward modification of case 1. Here are example data:

fig3_comp2dcorr

Figure 3

The bootstrap is done like this:

Nb = 500;
bootcorr1 = zeros(Nb,1);
bootcorr2 = zeros(Nb,1);

for B = 1:Nb

bootsample = randi(Np,1,Np);
bootcorr1(B) = Spearman(a1(bootsample),b1(bootsample),0);
bootcorr2(B) = Spearman(a2(bootsample),b2(bootsample),0);

end

alpha = 0.05; % probability coverage - 0.05 for 95% CI
hi = floor((1-alpha/2)*Nb+.5);
lo = floor((alpha/2)*Nb+.5);

% for each correlation
boot1sort = sort(bootcorr1);
boot2sort = sort(bootcorr2);
boot1ci = [boot1sort(lo) boot1sort(hi)]; 
boot2ci = [boot2sort(lo) boot2sort(hi)]; 

% for the difference between correlations
bootdiff = bootcorr1 - bootcorr2;
bootdiffsort = sort(bootdiff);
diffci = [bootdiffsort(lo) bootdiffsort(hi)];

We get:

corr(a1,b1) = 0.52 [0.34 0.66]
corr(a2,b2) = 0.56 [0.39 0.68]
difference = -0.04 [-0.24 0.17]

The difference is very close to zero and its confidence interval includes zero. So the training procedure is associated with a very weak change in correlation.

Instead of a confidence interval, we could also report a highest density interval, which will be very close to the confidence interval if the bootstrap distribution is symmetric – the Matlab script on github shows how to compute a HDI. We could also simply report the difference and its bootstrap distribution. This provides a good summary of the uncertainty we have about the difference, without committing to a binary description of the results as significant or not.

fig4_comp2dcorr

Figure 4

Conclusion

The strategies described here have been validated for Spearman’s correlation and the Winzorised correlation (Wilcox, 2016). The skipped correlation led to too conservative confidence intervals, meaning that in simulations, the 95% confidence intervals contained the true value more than 95% of the times. This illustrates an important idea: the behaviour of a confidence interval is always estimated in the long run, using simulations, and it results from the conjunction of an estimator and a technique to form the confidence interval. Finally, a very similar bootstrap approach can be used to compare regression coefficients (Wilcox 2012), for instance to compare the slopes of robust linear regressions in an overlapping case (Bieniek et al. 2013).

References

Bieniek, M.M., Frei, L.S. & Rousselet, G.A. (2013) Early ERPs to faces: aging, luminance, and individual differences. Frontiers in psychology, 4, 268.

Nieuwenhuis, S., Forstmann, B.U. & Wagenmakers, E.J. (2011) Erroneous analyses of interactions in neuroscience: a problem of significance. Nat Neurosci, 14, 1105-1107.

Pernet, C.R., Wilcox, R. & Rousselet, G.A. (2012) Robust correlation analyses: false positive and power validation using a new open source matlab toolbox. Front Psychol, 3, 606.

Wilcox, R.R. (2009) Comparing Pearson Correlations: Dealing with Heteroscedasticity and Nonnormality. Communications in Statistics-Simulation and Computation, 38, 2220-2234.

Wilcox, R.R. (2012) Introduction to robust estimation and hypothesis testing. Academic Press, San Diego, CA.

Wilcox, R.R. (2016) Comparing dependent robust correlations. Brit J Math Stat Psy, 69, 215-224.

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How to illustrate a 2×2 mixed ERP design

Let’s consider a simple mixed ERP design with 2 repeated measures (2 tasks) and 2 independent groups of participants (young and older participants). The Matlab code and the data are available on github. The data are time-courses of mutual information, with one vector time-course per participant and task. These results are preliminary and have not been published yet, but you can get an idea of how we use mutual information in the lab in recent publications (Ince et al. 2016a, 2016b; Rousselet et al. 2014). The code and illustrations presented in the rest of the post are not specific to mutual information.

Our 2 x 2 experimental design could be analysed using the LIMO EEG toolbox for instance, by computing a 2 x 2 ANOVA at every time point, and correcting for multiple comparisons using cluster based bootstrap statistics (Pernet et al. 2011, 2015). LIMO EEG has been used to investigate task effects for instance (Rousselet et al. 2011). But here, instead of ANOVAs, I’d like to focus on graphical representations and non-parametric assessment of our simple group design, to focus on effect sizes and to demonstrate how a few figures can tell a rich data-driven story.

First, we illustrate the 4 cells of our design. Figure 1 shows separately each group and each task: in each cell all participants are superimposed using thin coloured lines. We can immediately see large differences among participants and between groups, with overall smaller effects (mutual information) in older participants. There also seems to be task differences, in particular in young participants, which tend to present more sustained effects past 200 ms in the expressive task than the gender task.

fig1_gpmi2x2

Figure 1

To complement the individual traces, we can add measures of central tendency. The mean is shown with a thick green line, the median with a thick black line. See how the mean can be biased compared to the median in the presence of extreme values. The median was calculated using the Harrell-Davis estimator of the 50th quantile. To illustrate the group median with a measure of uncertainty, we can add a 95% percentile bootstrap confidence interval for instance (Figure 2).

fig2_gpmi2x2_ci

We can immediately see discrepancies between the median time-courses and their confidence intervals on the one hand, and the individual time-courses on the other hand. There are indeed many distributions of participants that can lead to the same average time-course. That’s why it is essential to show individual results, at least in some illustrations.

In our 2 x 2 design, we now have 3 aspects to consider: group differences, task differences and their interactions. We illustrate them in turn.

Age group differences for each task

We can look at the group differences in each task separately, as shown in Figure 3. The medians of each group is shown with 95% percentile bootstrap confidence intervals. On average, older participants tend to have weaker mutual information than young participants – less than half around 100-200 ms post-stimulus. This will need to be better quantified, for instance by reporting the median of all pairwise differences.

fig3_gpmi_group_diff

Figure 3

Under each panel showing the median + CI for each group, we plot the time-course of the group differences (young-older), with a confidence interval. For group comparisons we cannot illustrate individuals, because participants are be paired. However, we can illustrate all the bootstrap samples, shown in grey. Each sample was obtained by:

  • sampling with replacement Ny observations among Ny young observers
  • sampling with replacement No observations among No older observers
  • compute the median of each group
  • subtract the two medians

It is particularly important to illustrate the bootstrap distributions if they are skewed or contain outliers, or both, to check that the confidence intervals provide a good summary. If the bootstrap samples are very skewed, highest density intervals might be a good alternative to classic confidence intervals.

The lower panels of Figure 3 reveal relatively large group differences in a narrow window within 200 ms. The effect also appears to be stronger in the expressive task. Technically, one could also say that the effects are statistically significant, in a frequentist sense, when the 95% confidence intervals do not include zero. But not much is gained from that because some effects are large and others are small. Correction for multiple comparisons would also be required.

Task differences for each group

Figure 4 has a similar layout to Figure 3, now focusing on the task differences. The top panels suggest that the group medians don’t differ much between tasks, except maybe in young participants around 300-500 ms.

fig4_gpmi_task_effects

Figure 4

Because task effects are paired, we are not limited to the comparison of the medians between tasks; we can also illustrate the individual task differences and the medians of these differences [1]. These are shown in the bottom panels of Figure 4. In both groups, the individual differences are large and the time-courses of the task differences are scattered around zero, except in the young group starting around 300 ms, where most participants have positive differences (expressive > gender).

[1] When the mean is used as a measure of central tendency, these two perspectives are identical, because the difference between two means is the same as the mean of the pairwise differences. However, this is not the case for the median: the difference between medians is not the same as the median of the differences. Because we are interested in effect sizes, it is more informative to report descriptive statistics of the pairwise differences. The advantage of the Matlab code provided with this post is that instead of looking at the median, we can also look at other quantiles, thus getting a better picture of the strength of the effects.

Interaction between tasks and groups

Finally, in Figure 5 we consider the interactions between task and group factors. To do that we first superimpose the medians of the task differences with their confidence intervals (top panel). These traces are the same shown in the bottom panels of Figure 4. I can’t say I’m very happy with the top panel of Figure 5 because the two traces are difficult to compare. Essentially the don’t seem to differ much, except maybe for the late effect in young participants being higher than what is observed in older participants.

fig5_gpmi_task_group_interaction

In the lower panel of Figure 5 we illustrate the age group differences (young – older) between the medians of the pairwise task differences. Again confidence intervals are also provided, along with the original bootstrap samples. Overall, there is very little evidence for a 2 x 2 interaction, suggesting that the age group differences are fairly stable across tasks. Put another way, the weak task effects don’t appear to change much in the two age groups.

References

Ince, R.A., Jaworska, K., Gross, J., Panzeri, S., van Rijsbergen, N.J., Rousselet, G.A. & Schyns, P.G. (2016a) The Deceptively Simple N170 Reflects Network Information Processing Mechanisms Involving Visual Feature Coding and Transfer Across Hemispheres. Cereb Cortex.

Ince, R.A., Giordano, B.L., Kayser, C., Rousselet, G.A., Gross, J. & Schyns, P.G. (2016b) A statistical framework for neuroimaging data analysis based on mutual information estimated via a gaussian copula. Hum Brain Mapp.

Pernet, C.R., Chauveau, N., Gaspar, C. & Rousselet, G.A. (2011) LIMO EEG: a toolbox for hierarchical LInear MOdeling of ElectroEncephaloGraphic data. Comput Intell Neurosci, 2011, 831409.

Pernet, C.R., Latinus, M., Nichols, T.E. & Rousselet, G.A. (2015) Cluster-based computational methods for mass univariate analyses of event-related brain potentials/fields: A simulation study. Journal of neuroscience methods, 250, 85-93.

Rousselet, G.A., Gaspar, C.M., Wieczorek, K.P. & Pernet, C.R. (2011) Modeling Single-Trial ERP Reveals Modulation of Bottom-Up Face Visual Processing by Top-Down Task Constraints (in Some Subjects). Front Psychol, 2, 137.

Rousselet, G.A., Ince, R.A., van Rijsbergen, N.J. & Schyns, P.G. (2014) Eye coding mechanisms in early human face event-related potentials. J Vis, 14, 7.