Elsevier

NeuroImage

Volume 90, 15 April 2014, Pages 246-255
NeuroImage

Different topological organization of human brain functional networks with eyes open versus eyes closed

https://doi.org/10.1016/j.neuroimage.2013.12.060Get rights and content

Highlights

  • Both eyes-open and eyes-closed exhibit small-world properties.

  • The eyes act as a toggle between two distinct information processing modes.

  • The eyes act as a toggle between exteroceptive and interoceptive networks.

  • Cross-sensory modality connections are altered by volitional eye opening.

Abstract

Opening and closing the eyes are fundamental behaviors for directing attention to the external versus internal world. However, it remains unclear whether the states of eyes-open (EO) relative to eyes-closed (EC) are associated with different topological organizations of functional neural networks for exteroceptive and interoceptive processing (processing the external world and internal state, respectively). Here, we used resting-state functional magnetic resonance imaging and neural network analysis to investigate the topological properties of functional networks of the human brain when the eyes were open versus closed. The brain networks exhibited higher cliquishness and local efficiency, but lower global efficiency during the EO state compared to the EC state. These properties suggest an increase in specialized information processing along with a decrease in integrated information processing in EO (vs. EC). More importantly, the “exteroceptive” network, including the attentional system (e.g., superior parietal gyrus and inferior parietal lobule), ocular motor system (e.g., precentral gyrus and superior frontal gyrus), and arousal system (e.g., insula and thalamus), showed higher regional nodal properties (nodal degree, efficiency and betweenness centrality) in EO relative to EC. In contrast, the “interoceptive” network, composed of visual system (e.g., lingual gyrus, fusiform gyrus and cuneus), auditory system (e.g., Heschl's gyurs), somatosensory system (e.g., postcentral gyrus), and part of the default mode network (e.g., angular gyrus and anterior cingulate gyrus), showed significantly higher regional properties in EC vs. EO. In addition, the connections across sensory modalities were altered by volitional eye opening. The synchronicity between the visual system and the motor, somatosensory and auditory systems, characteristic of EC, was attenuated in EO. Further, the connections between the visual system and the attention, arousal and subcortical systems were increased in EO. These results may indicate that EO leads to a suppression of sensory modalities (other than visual) to allocate resources to exteroceptive processing. Our findings suggest that the topological organization of human brain networks dynamically switches corresponding to the information processing modes as we open or close our eyes.

Introduction

While vision has featured centrally in prominent scientific theories of consciousness (Crick and Koch, 2003), we spend a considerable portion of our lives with our eyes closed, thereby attenuating the potential contributions of vision. Interestingly, a recent study suggested that momentary closing of the eyes (blinking) not only occurs more often than would be necessary for ocular lubrication, but that these blinks are associated with subtle shifts in neural activity (Nakano et al., 2013). While awake, awareness shifts based on whether our eyes are open or closed; awareness has been described as “exteroceptive” when the eyes are open (EO) and “interoceptive” when the eyes are closed (EC). These states correspond to focus on the “outside” versus the “inside”, respectively, and each has different psychophysiological characteristics and underlying brain mechanisms (Marx et al., 2003).

Compared to EC, an increased attentional load and raised level of arousal is present in EO (Hufner et al., 2009). The differences attributable to these states may have more to do with the simple processing of visual information; even in the darkness, where little to no visual input is present, these two states reveal distinct neural activation patterns (Hufner et al., 2009). Attentional and oculomotor systems (e.g., superior parietal gyrus and frontal eye fields) show activation in EO, while sensory systems (e.g., visual, auditory, and somatosensory) show activation in EC (Bianciardi et al., 2009, Hufner et al., 2008, Hufner et al., 2009, Marx et al., 2003, Marx et al., 2004, McAvoy et al., 2008, Niven and Laughlin, 2008). These findings suggest two different states of mental activity: an “exteroceptive” state characterized by overt attention and ocular motor activity (during EO) and an “interoceptive” state characterized by imagination and multisensory activity (during EC) (Hufner et al., 2009, Marx et al., 2004). The corresponding differences of spontaneous neural activity between these two states have been characterized in previous resting-state functional magnetic resonance imaging (R-fMRI) studies (Bianciardi et al., 2009, McAvoy et al., 2008, Yan et al., 2009, Yang et al., 2007, Zou et al., 2009).

More recently, an R-fMRI study, by manipulating both eyes open/closed and lights on/off, found that there were significant differences between EO and EC in both spontaneous brain activity and functional connectivity but no differences in whole brain topological organization other than connection distance (i.e., the Euclidean distance between each pair of regional nodes) (Jao et al., 2013). Given that the topological properties of human brain networks have shown correlations with various cognitive functions and pathologies (Bullmore and Sporns, 2009, He and Evans, 2010), it is curious that there were widespread influences of EO and EC on the spontaneous activity and connectivity but not on the topological organization of the networks (Jao et al., 2013).

Given that there are critical influence of different acquisition parameters and analytic strategies in R-fMRI data but lacking consensus about the best way to deal with it (Murphy et al., 2009, Wang et al., 2009, Wig et al., 2011, Zuo et al., 2013), we acquired human R-fMRI data and constructed whole brain functional networks with different brain parcellation templates and presence/absence of global signal regression (GSR) to compare topological parameters (e.g., small-world, network efficiency and nodal efficiency) of brain networks between the EO and EC states. We hypothesized that the “exteroceptive” state and the “interoceptive” state were associated with different topological organizations of brain networks corresponding to different information processing modes. Specifically, we predicted that there would be an “exteroceptive” network, characterized by attention and ocular motor system during EO, and an “interoceptive” network characterized by imagination and multisensory system during EC.

Section snippets

Subjects

Twenty-three right-handed healthy volunteers (11 females; mean age ± SD, 20.17 ± 2.74 years) participated in this study. All participants were undergraduate/graduate students and had no history of neurological and psychiatric disorders or head injury. Written informed consent was obtained from each participant prior to the MRI acquisition. The study was approved by the Institutional Review Board of Beijing Normal University.

Data acquisition

MRI data were acquired on a Siemens Trio 3 T MRI scanner powered with a total

Global properties of the functional brain networks

Because topological properties of the obtained networks are affected by the choice of a specific sparsity value, setting a specific sparsity as the threshold can ensure that the networks corresponding to each subject have the same number of edges. To balance the prominent small-world attribute and the appropriate sparseness in brain functional networks across subjects, we set a series of threshold values for sparsity in the range of 0.10–0.28 at an interval of 0.01. This range of sparsity

Discussion

Although previous studies have attempted to investigate different neural presentations of exteroceptive and interoceptive states by manipulating the orientation of attention (Farb et al., 2013, Simmons et al., 2014), the easiest way to control the direction of visual attention as well as balances task difficulty, is simply eyes opened versus eyes closed, an approach which has been largely overlooked. Although previous fMRI studies have found different influences of EO and EC on regional brain

Acknowledgments

This work was supported by the Natural Science Foundation of China (Grant numbers: 91132704, 81071149, 81030028, 81271548, and 81371535), the National Basic Research Program of China (973 Program, 2011CB711000, 2014CB744600), the National Science Fund for Distinguished Young Scholars (Grant number: 81225012), and Scientific Research Foundation for the Returned Overseas Chinese Scholars (RH), and State Education Ministry of China. We thank Alexander Dufford for offering helpful comments.

Conflict

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