The current study aims to provide a step-by-step tutorial for calculating the magnitude of multisensory integration effects in an effort to facilitate the production of translational research studies across diverse clinical populations.
Multisensory integration research investigates how the brain processes simultaneous sensory information. Research on animals (mainly cats and primates) and humans reveal that intact multisensory integration is crucial for functioning in the real world, including both cognitive and physical activities. Much of the research conducted over the past several decades documents multisensory integration effects using diverse psychophysical, electrophysiological, and neuroimaging techniques. While its presence has been reported, the methods used to determine the magnitude of multisensory integration effects varies and typically faces much criticism. In what follows, limitations of previous behavioral studies are outlined and a step-by-step tutorial for calculating the magnitude of multisensory integration effects using robust probability models is provided.
Interactions across sensory systems are essential for everyday functions. While multisensory integration effects are measured across a wide array of populations using assorted sensory combinations and different neuroscience approaches [including but not limited to the psychophysical, electrophysiological, and neuroimaging methodologies]1,2,3,4,5,6,7,8,9, currently a gold standard for quantifying multisensory integration is lacking. Given that multisensory experiments typically contain a behavioral component, reaction time (RT) data is often examined to determine the existence of a well-known phenomenon called the redundant signals effect10. As its name suggests, simultaneous sensory signals provide redundant information, which typically yield quicker RTs. Race and co-activation models are used to explain the above mentioned redundant signals effect11. Under race models, the unisensory signal that is processed the fastest is the winner of the race and is responsible for producing the behavioral response. However, evidence for co-activation occurs when responses to multisensory stimuli are quicker than what race models predict.
Earlier versions of the race model are inherently controversial12,13 as they are referred to by some as overly conservative14,15 and purportedly contain limitations regarding the independence between the constituent unisensory detection times inherent in the multisensory condition16. In an effort to address some of these limitations, Colonius & Diederich16 developed a more conventional race model test:
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where the cumulative distribution frequencies (CDFs) of the unisensory conditions (e.g., A & B; with an upper limit of one) are compared to the CDF of the simultaneous multisensory condition (e.g., AB) for any given latency (t)11,16,17. In general, a CDF determines how often an RT occurs, within a given range of RTs, divided by the total number of stimulus presentations (i.e., trials). If the CDF of the actual multisensory condition is less than or equal to the predicted CDF derived from the unisensory conditions
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then the race model is accepted and there is no evidence for sensory integration. However, when the multisensory CDF is greater than the predicted CDF derived from the unisensory conditions, the race model is rejected. Rejection of the race model indicates that multisensory interactions from redundant sensory sources combine in a non-linear manner, resulting in a speeding up of RTs (e.g., RT facilitation) to multisensory stimuli.
One main hurdle that multisensory researchers face is how to best quantify integration effects. For instance, in the case of the most basic behavioral multisensory paradigm, where participants are asked to perform a simple reaction time task, information regarding accuracy and speed is collected. Such multisensory data can be used at the face-value or manipulated using various mathematical applications including but not limited to Maximum Likelihood Estimation18,19, CDFs11, and various other statistical approaches. The majority of our previous multisensory studies employed both quantitative and probabilistic approaches where multisensory integrative effects were calculated by 1) subtracting the mean reaction time (RT) to a multisensory event from the mean reaction time (RT) to the shortest unisensory event, and 2) by employing CDFs to determine whether RT facilitation resulted from synergistic interactions facilitated by redundant sensory information8,20,21,22,23. However, the former methodology was likely not sensitive to the individual differences in integrative processes and researchers have since posited that the later methodology (i.e., CDFs) may provide a better proxy for quantifying multisensory integrative effects24.
Gondan and Minakata recently published a tutorial on how to accurately test the Race Model Inequality (RMI) since researchers all too often make countless errors during the acquisition and pre-processing stages of RT data collection and preparation25. First, the authors posit that is unfavorable to apply data trimming procedures where certain a priori minimum and maximum RT limits are set. They recommend that slow and omitted responses be set to infinity, rather than excluded. Second, given that the RMI may be violated at any latency, multiple t-tests are often used to test the RMI at different time points (i.e., quantiles); unfortunately, this practice leads to the increased Type I error and substantially reduced statistical power. To avoid these issues, it is recommended that the RMI be tested over one specific time range. Some researchers have suggested that it makes sense to test the fastest quartile of responses (0-25%)26 or some pre-identified windows (i.e., 10-25%)24,27 as multisensory integration effects are typically observed during that time interval; however, we argue that the percentile range to be tested must be dictated by the actual dataset (see Protocol Section 5). The problem with relying on published data from young adults or computer simulations is that older adults manifest very different RT distributions, likely due to the age-related declines in sensory systems. Race model significance testing should only be tested over violated portions (positive values) of group-averaged difference wave between actual and predicted CDFs from the study cohort.
To this end, a protective effect of multisensory integration in healthy older adults using the conventional test of the race model16 and the principles set forth by Gondan and colleagues25 has been demonstrated. In fact, greater magnitude of visual-somatosensory RMI (a proxy for multisensory integration) was found to be linked to better balance performance, lower probability of incident falls and increased spatial gait performance28,29.
The objective of the current experiment is to provide researchers with a step-by-step tutorial to calculate the magnitude of multisensory integration effects using the RMI, to facilitate the increased production of diverse translational research studies across many different clinical populations. Note that data presented in the current study are from recently published visual-somatosensory experiments conducted on healthy older adults28,29, but this methodology can be applied to various cohorts across many different experimental designs, utilizing a wide-array of multisensory combinations.
All participants provided written informed consent to the experimental procedures, which were approved by the institutional review board of the Albert Einstein College of Medicine.
1. Participant Recruitment, Inclusion Criteria, and Consent
2. Experimental Design
3. Apparatus & Task
4. Race Model Inequality Data Preparation (Individual Level)
5. Quantification of the Multisensory Effect (Group Level).
The purpose of this study was to provide a step-by-step tutorial of a methodical approach to quantify the magnitude of VS integration effects, to foster the publication of new multisensory studies using similar experimental designs and setups (see Figure 1). Screenshots of each step and calculation needed to derive magnitude of multisensory integration effects, as measured by RMI AUC, are delineated above and illustrated in Figures 2-8.
Figure 9 demonstrates a group-averaged violation (dashed trace) occurring over the 0-10% percentile range for a sample of 333 older adults (see also29). Here, the total number of positive values (0, 1, 2, or 3) for those 3 quantiles (0.00 – 0.10) determines which multisensory classification group a person is assigned (deficient, poor, good, or superior) respectively.
As depicted in Figure 9, group-averaged results demonstrate a significant race model violation over the fastest tenth of all response times26. While this group-averaged difference waveform suggests that on average older adults demonstrate significant race model violation (i.e., multisensory integration effects), we argue that this is not a one size fits all model. Rather, the individual’s AUC under the violated time period (0-10%ile) provides a better proxy for assessing the individual’s magnitude of VS integration, as differential integration patterns have been documented 20-23, 28,29. Once calculated, the individual magnitude of VS integration can serve as a continuous predictor of important outcomes in various clinical populations.
We recommend implementing a classification system, perhaps based on the number of violated percentile bins (values greater than zero) during the group-averaged RMI violation period, as a means of depicting inherent differential integration patterns. Classification of data in this manner will reveal a clear degradation of race model violation by multisensory integration classification group.
Figure 1: Experimental apparatus. Using a foot pedal located under the right foot as a response pad, participants were asked to respond to unisensory and multisensory stimuli as quickly as possible. This figure has been reprinted with permission22,28,29. Please click here to view a larger version of this figure.
Figure 2: Calculating the frequency of an RT occurring within a specified range of RTs for each experimental condition. a) Visual (V); b) Somatosensory (S); and c) Visual-Somatosensory (VS). Please click here to view a larger version of this figure.
Figure 3: Creating the cumulative distribution frequency for the experimental conditions. This figure depicts the summation of the cumulative probability at the 95%ile bin for the Soma (S) condition. Please click here to view a larger version of this figure.
Figure 4: Plotting the Actual CDF (VS condition; purple trace) as a function of quantile. Please click here to view a larger version of this figure.
Figure 5: Calculating the Predicted CDF. Sum the CDFs of the two unisensory CDFs while including an upper limit = 1 for each of the quantiles from 0.00 to 1.00. Please click here to view a larger version of this figure.
Figure 6: Create the Race Model Inequality (RMI). Subtract the CDF of the predicted CDF from the actual CDF for each quantile. Please click here to view a larger version of this figure.
Figure 7: Plot the individual RMI values. The x-axis represents each of the 21 quantiles (column AC) and the y-axis represents the probability difference between CDFs (column AH). The green highlighted portion of the RMI depicts the positive or violated portion of the waveform, indicative of multisensory integration. Please click here to view a larger version of this figure.
Figure 8: Calculating an individual’s Area-Under-the-Curve (AUC). a) Sum the CDF difference value at quantile 1 (0.00) with the CDF difference value of quantile 2 (0.05) and then divide by two to create a measure of AUC from 0.00 – 0.05. b-c) Repeat step a) for each consecutive pair of quantiles (e.g., 0.05 – 0.10 and 0.10 – 0.15) to attain the AUC for each quantile range. d) Sum the AUC for each time bin range to obtain the total AUC for the entire time bin window identified in 5.3. Note this example includes a wider quantile range (0.00 – 0.15) for illustrative purposes only. Please click here to view a larger version of this figure.
Figure 9: Race Model Inequality: Overall and by Group Classification. The group-averaged difference between actual and predicted CDFs over the trajectory of all quantiles is represented by the dashed trace. The solid traces represent each of the four multisensory integration classifications defined above based on the number of violated quantile bins. This adapted figure has been reprinted with permission29. Please click here to view a larger version of this figure.
Supplementary File 1: Sample Simple Reaction Time Paradigm programmed in Eprime 2.0. Please click here to download this file.
Supplementary File 2: Sample RT data behavioral data output from Eprime 2.0. Please click here to download this file.
Supplementary File 3: Sample RMI data with and without outliers and omitted trials. Please click here to download this file.
Table 1. Individual Descriptive Statistics by Condition and Calculation of RT Range. Please click here to download this file.
Table 2. Example of how to bin RT data based on RT range. Please click here to download this file.
Table 3. Example of AUC calculation & Identification of # of violated quantiles (grey shaded area). Please click here to download this file.
The goal of the current study was to detail the process behind the establishment of a robust multisensory integration phenotype. Here, we provide the necessary and critical steps required to acquire multisensory integration effects that can be utilized to predict important cognitive and motor outcomes relying on similar neural circuitry. Our overall objective was to provide a step-by-step tutorial for calculating the magnitude of multisensory integration in an effort to facilitate innovative and novel translational multisensory studies across diverse clinical populations and age-ranges.
As stated above and outlined by Gondan and colleagues, it is very important to preserve the individual’s RT dataset25,28. That is, avoid data trimming procedures that omit very slow RTs given its inherent bias on the RT distribution;25 instead, set omitted and slow RTs to infinity. This step is critical and failure to abide by these simple rules will lead to the development of inaccurate multisensory integration results. Additionally, race model significance testing should only be tested over group-averaged violated portions of the RMI identified in the study cohort (i.e., not a priori specified windows).
In terms of limitations, the current experimental design was based on data from a simple reaction time task to bilateral stimuli that were presented to the same location and at precisely the same time. We recognize that several adaptations to the current experimental design can be made depending upon various hypotheses that researchers are interested in examining. We utilize this study as a launching pad towards documenting robust MSI effects in aging but recognize that implementation of various experimental adaptations (e.g., different bi- and even tri-sensory combinations, varied stimulus presentation onset times, and differential magnitude of stimulus intensity) will provide a wealth of incremental information regarding this multisensory phenomenon.
We have implemented the above approach to demonstrate significant associations between the magnitude of visual-somatosensory integration with balance28 and incident falls28, where older adults with greater multisensory integration abilities manifest better balance performance and less incident falls. Similarly, we demonstrate that the magnitude of visual-somatosensory integration was a strong predictor of spatial aspects of gait29, where individuals with worse visual-somatosensory integration demonstrated slower gait speed, shorter strides, and increased double support. In the future, this methodology should be used to uncover the relationship of MSI with other important clinical outcomes like cognitive status, and aid in the identification of critical functional and structural multisensory integrative neural networks in aging and other clinical populations.
The authors have nothing to disclose.
The current body of work is supported by the National Institute on Aging at the National Institute of Health (K01AG049813 to JRM). Supplementary funding was provided by the Resnick Gerontology Center of the Albert Einstein College of Medicine. Special thanks to all the volunteers and research staff for exceptional support with this project.
stimulus generator | Zenometrics, LLC; Peekskill, NY, USA | n/a | custom-built |
Excel | Microsoft Corporation | spreadsheet program | |
Eprime | Psychology Software Tools (PST) | stimulus presentation software |