Decreased Connectivity in Left Frontal Orbital Cortex After Sleep

Deprivation

Aoke Zheng

1,2

, Yan He

2,*

and Hao Yan

2,*

College of English Studies, Xi’an International Studies University, Xi’an, China

Key Laboratory for Artificial Intelligence and Cognitive Neuroscience of Language, Xi’an International Studies

University, Xi’an, China

Keywords: Sleep Deprivation, Anger, gPPI, Brain Network.

Abstract: Men are reported to be likely to express more anger than women. Insufficient sleep may lead to cognitive

changes, and most adults are plagued by this problem. Researches have proved that lack of sleep can cause

the emotion of anger. However, the neural mechanisms of this phenomenon still need to be discovered.

Aiming to explore why men tend to experience anger after sleep deprivation (SD) by utilizing the method of

brain network science, a generalized PsychoPhysiological Interaction (gPPI) analysis was administered. A

total of 18 male participants were enrolled in this study. As a vital area for regulating emotions, the left frontal

orbital cortex (FOrb) showed decreased connectivity to the posterior cingulate gyrus (PC) and cerebellum,

while PC and cerebellum are known to involve in emotion regulation. Decreased connectivity in these areas

might provide a plausible explanation for how SD influences male to process the emotion of anger. Our results

provide further evidence that sleep deprivation is closely related to the emotion of anger and the adoption of

brain network science offers new insights in uncovering the neural mechanism for SD’s impact on men’s

processing of anger.

1 INTRODUCTION

Humans spend approximately one-third of their lives

asleep. (Farahani et al., 2019). Previous researches

indicate that emotional abilities are fairly disrupted

due to sleep deprivation (Krause et al., 2017).

According to Saghir et al (2018), sleep deprivation

leads to the bursts of anger. Anger is a syndrome of

relatively specific feelings; certain physiological

reactions are urged to damage some target (Berkowitz

et al., 2004). Although it has great impact on our daily

life, it remains one of the least studies of the basic

emotions (Alia-Klein et al., 2020). Men are more

emotionally reactive to anger, and this can trigger

more aggressive tendencies (Potegal et al., 2004;

Iverson et al., 2019, Kim et al., 2022; Fernández-

Modamio et al., 2020). Potegal and Archer (2004)

demonstrated that men were more frequently the

targets of anger than women. Iverson et al. (2019)

illustrated that a significant minority of middle-aged

men reported some degree of anger and aggression,

which are correlated with depression and anxiety.

Kim et al. (2022) illustrated that men tend to be more

aggressive than women when they experience the

same level of anger. Fernández-Modamio et al.

(2020) found that men recognized disgust and neutral

expressions better than women. Previous studies have

proved that men experience more anger, which leads

to acute consequences for their life quality. However,

most studies focus on questionnaire survey, it is

necessary to probe into the influence of anger by way

of objective measurements.

Previous neuroimaging researches based on

functional magnetic resonance imaging (fMRI), a

non-invasive technique to observe activation or

connectivity activity of the brain, also demonstrated

that emotion functions were greatly influenced by

sleep deprivation. By means of brain networks,

self-organized associations are revealed among

various brain regions in order to accomplish different

cognition functions. Under the condition of sleep

deprivation, the functional connectivity between the

amygdala and the ventral anterior cingulate cortex

(vACC) was significantly decreased, which resulted

in aggravation of subjective mood including anger

(Motomura et al., 2013). Resting-state functional

Zheng, A., He, Y. and Yan, H.

Decreased Connectivity in Left Frontal Orbital Cortex After Sleep Deprivation.

DOI: 10.5220/0011929300003612

In Proceedings of the 3rd International Symposium on Automation, Information and Computing (ISAIC 2022), pages 367-371

ISBN: 978-989-758-622-4; ISSN: 2975-9463

 2023 by SCITEPRESS – Science and Technology Publications, Lda. Under CC license (CC BY-NC-ND 4.0)

367

MRI (fMRI) was used to examine the changes in

functional connectivity of the basolateral amygdala

(BLA) and centromedial amygdala (CMA) following

sleep deprivation (Shao et al., 2014). The findings

indicated that a lack of sleep led to a significant

decrease in the functional connectivity between the

basolateral amygdala (BLA) and various executive

control regions. These studies demonstrated that sleep

deprivation may worsen anger emotional states.

In short, males are affected by anger to a great

extent, and sleep deprivation has effect on men’s

negative emotion like anger, while the underlying

neural mechanism is not clear. In this paper, we

adopted Stockholm Sleepy Brain Research to reveal

how sleep deprivation affect men’s angry emotion

processing.

2 METHODS

2.1 Study Design

Neuroimaging data used in this study were obtained

from the Stockholm Sleepy Brain Project which is

publicly available as one OpenNEURO database

(Tamm, 2019). The study was a randomized

crossover design with the interval of one month. They

underwent fMRI scanning under full sleep and 3-hour

sleep deprivation with the interval of one month in a

counterbalanced order. The experiment employed

three different emotional paradigms, and two resting

state sessions.

2.2 Participants

Participants filled out an online screening form after

being recruited through the website, posters and a

newspaper advertisement (Nilsonne et al., 2017). In

this study, a total of 18 males are enrolled. All of them

passed the inclusion criteria, including no psychiatric

or neurological illness, no working or studying

experience in psychology, behavioral science or

medicine, no color blind, and all right-handed. They

also completed the insomnia severity index (ISI) to

test the insomnia symptoms, and the Karolinska Sleep

Questionnaire (KSQ) to test the sleep patterns.

Besides, the Hospital Anxiety and Depression Scale

(HADS) was used to test the depressive symptoms.

2.3 Experimental Paradigm

The Karolinska Directed Emotional Faces (KDEF)

database served for the source of the experiment

materials (Lundqvist et al., 1998). The study

employed happy, neutral and angry emotional

pictures in a block design. Every block lasted for 20

seconds and 20 faces were included, each of which

was displayed for 0.5 seconds. In total, there were 12

blocks of images (4 happy, 4 angry and 4 neutral).

They were organized in groups of three, such as

happy-neutral-happy or angry-neutral-angry.

Participants were required to grade how happy and

angry they felt on a visual analog scale of 0-100 after

each set of three (Nilsonne et al., 2017).

2.4 Data Acquisition

fMRI data were obtained from a 3T Discovery 750

MRI scanner (General Electric) with an 8-channel

head coil. T1-weighted anatomical scans were

acquired with a sagittal BRAVO (brain volume

imaging) sequence, TR=6.4ms, TE=2.81ms,

inversion time=0.45ms, FA=11°, FOV=240mm ◊

240 mm◊180mm, 180 slices, slice thickness=1 mm,

interleaved bottom-up. Functional scans were

acquired in a gradient echo-planar-imaging (EPI)

sequence, TR=3000ms, TE=34ms, FA=80°,

FOV=220 mm◊220 mm◊110mm, 46 slices, slice

thickness=2.3mm, interleaved bottom-up.

2.5 fMRI Preprocessing and Analysis

To investigate task-modulated changes in

connectivity, we performed generalized

PsychoPhysiological Interaction (gPPI) measures.

gPPI is a special type of multiple regression that

includes a psychological regressor, a physiological

regressor, and a condition specific interaction

regressor, which reveals whether the functional

connectivity between separate nodes depending on

what task the participant is currently doing. Its

computation comes from multiple regression model

corresponding with each individual ROI (Region of

Interest) time series. Each time course was

deconvolved and then its output was regarded as

physiological regressors. In detail, the experimental

conditions of emotion contagion were taken as

psychological regressors. The interactions between

the time-courses of ROI seeds and the experimental

conditions were used as PPI regressors, which were

convolved with HRF, and different β values were

generated, as presented in Figure 1.

Data were analyzed in CONN toolbox V.20.b.

(Whitfield-Gabrieli, 2012). Functional images were

first

realigned, where all scans are coregistered and

ISAIC 2022 - International Symposium on Automation, Information and Computing

368

Figure 1: gPPI analysis process.

resampled to a reference image. Next, temporal

misalignment was corrected by slice-timing. Outlier

identification was then applied to identify potential

outlier scans. Later, structural and functional data

were segmented into grey matter, white matter, and

CSF tissue classes and normalized into standard MNI

space (Ashburner et al., 1997). The functional data

was then smoothed using spatial convolution with a

Gaussian kernel of 8mm full width half maximum

(FWHM). Subsequently, the denoising step, which

applies linear regression and band-pass filtering, was

used to remove unwanted motion, physiological, and

other artifactual effects from the BOLD signal (Nieto-

Castanon, 2020). In the end, a paired t-test were

conducted to compare functional connectivity

between full sleep and sleep-deprived conditions.

3 RESULTS

According to the paired t-test, significant effects

emerged in the left frontal orbital cortex (LFOrb). As

demonstrated in Figure 2, the functional connectivity

between LFOrb and the posterior cingulate gyrus

(PC) was decreased after sleep deprivation. In

addition, the functional connectivity between LFOrb

and left Cerebellum was decreased. Decreased

connectivity was also found between left amygdala

and right hippocampus. Moreover, some visual areas

such as right occipital pole and right frontal eye fields

showed decreased connectivity. Increased

connectivity was found between right rostral

prefrontal cortex and left frontal pole. Besides, the

right occipital fusiform gyrus showed increased

connectivity with left temporal occipital fusiform

cortex. The same results were not found under happy

condition.

Figure 2: Decreased functional connectivity between left

frontal orbital cortex and posterior cingulate gyrus (LPC),

left Cerebellum 8.

4 DISCUSSION

According to the experimental results, the paired t-

test showed significant effects in the left frontal

orbital cortex (LFOrb) and posterior cingulate gyrus

(PC). Previous researches indicated that men were

facing with sleep problems and had difficulties in

dealing with anger emotion simultaneously. This

study intended to decipher the neural mechanisms

underlying these phenomena. Results suggested

significant effects in the left frontal orbital cortex

(LFOrb) seed. Specifically, after sleep deprivation,

the functional connectivity between LFOrb and

posterior cingulate gyrus (PC) was decreased. In

addition, the functional connectivity between LFOrb

and left Cerebellum 8 was decreased.

As a crucial area for regulating emotion, the

orbitofrontal area represents one critical structure in a

neural system serving decision making (Arnsten et al.,

2012; Bechara et al., 2000). Decreased connectivity

ROI BOLD

timecourse

deconvolve

physiological

regressors

interaction

PPI

regressors

convolved with

HRF

β values

task

psychological

regressors

psychological

regressors

interaction

PPI

regressors

Decreased Connectivity in Left Frontal Orbital Cortex After Sleep Deprivation

369

of OFC would impair stimulus‐reward reversal

learning, response inhibition, and ability to balance

the appropriateness of their behavior in the social

context (Viskontas et al., 2007). Research has shown

that there are changes in risk-taking behavior

following sleep deprivation, bringing about more

dangerous or risky decisions (Womack et al., 2013).

Lack of sleep enhances the sensitivity of reward

system. Negative emotional experiences are

associated with the activation of the reward network,

including orbitofrontal cortex. Posterior cingulate

cortex plays a critical role in the default mode

network. It receives strong feedback from areas

involved in emotion processing and social behavior,

including the orbital frontal cortex (Maddock et al.,

2003). Cerebellum is in control of the arousal and

reward system. The abnormal activation in this area

might also influence the ability to deal with the

negative emotion. Decreased connectivity in these

areas might be able to explain why SD significantly

influenced the emotion of anger of men.

Our results also found decreased connectivity

between left amygdala and right hippocampus.

Amygdala-hippocampus interactions allow for

emotional processing in the amygdala to influence

memory storage in the hippocampus, thereby

mediating emotional memories’ consolidation and

retrieval. (Kirby et al., 2018; Yang et al., 2017;

Roesler et al., 2021; Fastenrath et al., 2014). Yang et

al. (2017) proposed that the amygdala and

hippocampus can act synergistically to regulate

emotion-based memories. The findings of a fMRI

study suggest that the amygdala may be instrumental

in regulating how emotional information is stored in

the hippocampus. The study found that the connection

between the amygdala and hippocampus is much

stronger when emotionally positive or negative

pictures are being encoded (Fastenrath et al., 2014).

Decreased functional connectivity between the

amygdala and hippocampus may indicate that sleep

deprivation impairs male’s ability of angry emotional

memory retrieval and consolidation.

Sleep is an essential part of our life. Insufficient

sleep could correlate with anger, which may lead to

aggressive behaviors. It is of great importance to

study the effect of sleep deprivation on anger. This

study took males as participants and focused on how

sleep deprivation influences angry emotion, which

shed light on the study of male’s emotion and sleep

problems. However, this study did not investigate

whether the same results exist in females. Further

studies can make a comparison between males and

females to depict gender differences in angry emotion

processing under the condition of sleep deprivation.

ACKNOWLEDGMENTS

This work was supported partly by the Basic Research

Program for the Natural Science of Shaanxi Province

of China under Grant 2019JQ861 and Grant

2022JM134. This work was partly supported by the

start-up foundation from Xi’an International Studies

University (Grant no. KYQDF202138).

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