Elsevier

NeuroImage

Volume 63, Issue 1, 15 October 2012, Pages 212-222
NeuroImage

Between-brain connectivity during imitation measured by fNIRS

https://doi.org/10.1016/j.neuroimage.2012.06.028Get rights and content

Abstract

The present study aimed to step into two-person neuroscience by investigating the hemodynamic correlates of between-brain connectivity involved in imitation and its dependency on pacing stimuli. To test this approach, we used wireless functional near-infrared spectroscopy (fNIRS) to record simultaneously during imitation performance of a paced finger-tapping task (PFT) in two subjects over premotor cortices (PMC). During the imitation (IM) condition, a model and an imitator were recorded while tapping in synchrony with auditory stimuli separated by a constant interval (stimulus-paced mode, St-P), followed by tapping without the pacing stimulus (self-paced mode, Se-P). During the control (CO) condition, each subject (single 1 and 2) performed the PFT task with the same pacing mode pattern, but alone without reference to each other.

Using wavelet transform coherence (WTC) analysis evaluating functional connectivity between brains, we found (1) that IM revealed a larger coherence increase between the model and the imitator as compared to the CO condition. (2) Within the IM condition, a larger coherence increase was found during Se-P as compared to St-P mode. Using Granger-causality (G-causality) analysis evaluating effective connectivity between brains, we found (3) that IM revealed larger G-causality as compared to the CO condition and (4) that within the IM condition, the signal of the model G-caused that of the imitator to a greater extent as compared to vice versa.

Our findings designate fNIRS as suitable tool for monitoring between-brain connectivity during dynamic interactions between two subjects and that those measurements might thereby provide insight into activation patterns not detectable using typical single-person experiments. Overall, the results of the present study demonstrate the potential of simultaneously assessing brain hemodynamics in interacting subjects in several research areas where social interactions are involved.

Highlights

► Imitation task vs control task was measured simultaneously in two subjects by fNIRS. ► fNIRS reflects increased between-brain connectivity during imitation versus control. ► fNIRS reflects increased Granger-causality during imitation versus control. ► fNIRS can be used for two-person neuroscience approaches.

Introduction

Human imitation refers to the ability to imitate other's sequences of movements or behaviors after one or just a few viewings. Imitation has been shown to play a crucial role such as in infant development (Ray and Heyes, 2011), social cognition (Iacoboni, 2009) and neurorehabilitation (Garrison et al., 2010). According to the so-called simulation hypothesis (Jeannerod, 1994, Rizzolatti et al., 2001), imitation activates a cortical network located in primary motor cortex (M1) and secondary motor areas, such as premotor cortex (PMC), supplementary motor area (SMA) and parietal cortices (Fadiga et al., 1995) which is thought to overlap with those areas responsible for motor execution of the same action (Decety, 1996, Lotze et al., 1999).

The majority of previous neuroimaging studies investigating imitation focused on the role of the imitator, partially due to practical limitations to use neuroscientific methods simultaneously in two interacting subjects (Arbib et al., 2000, Iacoboni, 2006, Molenberghs et al., 2009). However, recording both roles, i.e. the model and the imitator, in an attempt to elucidate the between-individual neural mechanisms of human imitating interaction remains an open challenge and an objective of moving toward two-person neuroscience (Dumas et al., 2010, Hari and Kujala, 2009). To conduct brain imaging in imitation interactions, a neuroimaging method is required that allows for simultaneous investigation of two brains, i.e. the model and the imitator.

To realize this new approach, we used functional near-infrared spectroscopy (fNIRS), an optical brain imaging method that has been shown in a previous study to represent a suitable experimental vehicle to investigate two interacting brains. Cui et al. recorded simultaneously in two people while playing a computer-based cooperation game side by side. The authors found that the inter-brain activity coherence between signals generated by participants' right superior frontal cortices increased during cooperation, but not during competition. Increased coherence was also associated with better cooperation performance (Cui et al., 2012).

In the present study a novel miniaturized wireless fNIRS instrument was used (Muehlemann et al., 2008). In contrast to traditional neuroimaging methods, such as functional magnetic resonance imaging (fMRI) and positron emission tomography (PET), our fNIRS technology offers a wireless and portable instrument that do not require a user's body or head to be restrained, and can therefore be used as a brain monitoring tool in everyday settings. Hence, we hypothesized that our wireless fNIRS device could overcome some of the limitations inherent to traditional neuroimaging methods and considered it a suitable tool for a new approach investigating both the model's and the imitator's brain.

In summary, the aim of the study was to (1) record between-brain hemodynamics during imitation of finger-tapping movements simultaneously in a model and an imitator using fNIRS. (2) We further aimed to evaluate whether the pacing mode during imitation, i.e. stimulus-paced versus self-paced, has an effect on between-brain hemodynamics. (3) To analyze the data obtained in terms of between-brain connectivity we aimed to apply two different approaches, i.e. WTC parsing functional connectivity and G-causality parsing causal connectivity.

Section snippets

Subjects

16 subjects were assigned as eight experimental pairs each consisting of a model and an imitator. All subjects (models: four females, mean age (± STD) 27.13 ± 4.22; imitators: 3 females, mean age 28.25 ± 4.23) were right-handed (models: mean laterality quotient (LQ ± STD) = 80.88 ± 20.75; imitators: mean LQ = 76.50 ± 11.20) according to the Edinburgh Handedness Inventory (Oldfield, 1971). There were no significant differences between models and imitators in terms of sex, age or handedness. Exclusion criteria

fNIRS data processing

A program was written in MATLAB® (Version 2008a) to pre-process the raw light intensity values. By applying the modified Beer–Lambert law (MBLL), from the measured absorption changes of NIR light after its transmission through tissue the concentration over time for oxy-hemoglobin (O2Hb) and deoxy-hemoglobin (HHb) ([O2Hb], [HHb]) was computed, which represent the dominant light absorber for living tissue in the NIR spectral band (Delpy et al., 1988). First, the NIRS signals were sampled at 100 Hz

Functional connectivity (wavelet transform coherence (WTC))

Fig. 3 illustrates an exemplary pair of two subjects over all channels 1–4. In Fig. 3 (A, Top), which is representing the IM condition, two frequency bands with high coherence (indicated in red colors) were found: first, high coherence values were found in the frequency band from 0.5 Hz to 0.25 Hz (corresponding to period between 2 s and 4 s). This frequency band includes the period of the finger-tapping (0.3 Hz corresponding to period ~ 3 s) indicating that this coherence increase is task-related.

Discussion

We present fNIRS data recorded in pairs of two subjects simultaneously during imitation of stimulus-paced (St-P) versus self-paced (Se-P) finger-tapping movements. Using wavelet transform coherence (WTC) analysis evaluating functional connectivity between brains, we found (1) that the IM condition revealed a larger coherence increase between the model and the imitator as compared to the CO condition. (2) Within the IM condition, a larger coherence increase was found during Se-P as compared to

Conclusion

Our findings provide insight in between-brain connectivity during imitation of stimulus-paced (St-P) versus self-paced (Se-P) finger-tapping movements recorded using fNIRS in two individuals simultaneously. Using wavelet transform coherence (WTC) analysis evaluating functional connectivity between brains, we found (1) that the IM condition revealed a larger coherence increase between the model and the imitator as compared to the CO condition. (2) Within the IM condition, a larger coherence

Acknowledgment

The authors thank all participants for assistance in carrying out this research and the Forschungskredit, University of Zurich, and the Stiftung für wissenschaftliche Forschung, University Zurich for financial support.

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