The Effects of Inaudible Binaural Beats on Visuospatial Memory: An fNIRS Study

The Effects of Inaudible Binaural Beats on Visuospatial Memory: An fNIRS Study | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article The Effects of Inaudible Binaural Beats on Visuospatial Memory: An fNIRS Study Ji-Su Kim, Kyu-Beom Kim, Yong-Bin Jeong, Min-Kyun Lee, Mi-Hyun Choi, and 2 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4167182/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 16 Oct, 2024 Read the published version in Scientific Reports → Version 1 posted 10 You are reading this latest preprint version Abstract This study aimed to observe the impact of pure Binaural Beats (BB) stimulation in the inaudible frequency range, excluding the influence of sound, on visuospatial memory. Additionally, we investigated whether the brainwave changes induced by BB stimulation directly affect brain activation. The experiment involved 17 participants (12 males with a mean age of 23.2 ± 1.7 and 5 females with a mean age of 21.0 ± 0.7) in their 20s. Each participant received 10 Hz BB stimulation by presenting frequencies of 18000 Hz and 18010 Hz to the left and right ears, respectively. The experiment consisted of Rest phase (5min), Task phase (5min), and Rest phase (5min). The Task phase included conditions where participants performed the task either without BB stimulation "Task only" or with BB stimulation "Task + BB". Visuospatial memory was evaluated using the 3-back task. To observe brain activation, functional Near Infrared Spectroscopy (fNIRS) was employed to measure hemodynamic responses in all phases. The cognitive task performance (Accuracy, Reaction time) and oxyhemoglobin (HbO) concentration during the Task phase were compared between conditions with and without BB stimulation using paired t-tests. Results indicated a significantly shorter Reaction time in the Task + BB condition compared to the Task only condition. Moreover, an increase in HbO concentration was observed in the F1-F3, F2-F4, and P2-P4 regions during the Task + BB condition. In conclusion, the observed increase in HbO concentration suggests a positive influence on task performance. This study is meaningful in objectively demonstrating the impact of inaudible BB stimulation on visuospatial memory, utilizing both behavioral data and direct neural activation reflected in hemodynamic responses. Biological sciences/Neuroscience Health sciences/Health care Binaural Beats fNIRS cerebral hemodynamic visuospatial memory Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 1. Introduction Binaural Beats (BB) refer to auditory stimuli presented to both ears with different frequencies, inducing brainwave synchronization at the frequency difference [ 1 ]. For example, presenting a 100 Hz base frequency to one ear and a BB stimulus with a base frequency plus a differential frequency of 110 Hz to the other ear would synchronize brainwaves at the differential frequency of 10 Hz [ 2 ]. Numerous studies have provided evidence supporting the positive effects of BB-induced brainwave entrainment on cognitive aspects [ 3 – 5 ]. However, conflicting results suggesting no improvement in cognitive function due to BB stimulation have also been reported [ 6 – 8 ]. The divergent outcomes in the effects of BB are expected to be attributed to various reasons, and one contributing factor could be the use of audible BB stimuli in previous studies, potentially impacting cognitive processing with sounds in the audible range [ 9 – 11 ]. Our research team addressed this issue by eliminating the influence of audible sounds in prior studies and observed the brainwave entrainment effects of BB. Specifically, we validated the ability of inaudible BB with a base frequency of 18000 Hz and a differential frequency of 10 Hz to induce alpha waves [ 12 ]. Additionally, when evaluating visuospatial memory performance while presenting inaudible BB stimuli, we found an enhancement in task performance compared to conditions without stimulation, demonstrating the positive impact of pure BB stimuli on cognitive processing [ 13 ]. However, all previous studies, including our team's prior research, focused solely on observing changes in brainwaves based on rhythmic neural activity and did not directly observe brain activity. Therefore, studies directly observing the effects of BB on cognitive processes related to brain activation, such as changes in neural activity or cerebral blood flow, are currently lacking. To further validate the scientific impact of BB effects, additional research involving direct observation of brain neural activity is crucial. Hence, in this study, we aim to reexamine the impact of inaudible BB stimulation, free from the influence of sound, using a base frequency of 18000 Hz and a differential frequency of 10 Hz. Simultaneously, we seek to observe brain activation responses. We selected visuospatial memory, a representative cognitive task, and employed functional Near Infrared Spectroscopy (fNIRS), a convenient method for measuring brain hemodynamic responses closely associated with changes in brain activity. 2. Methods 2.1. Subjects We recruited a total of 17 healthy individuals in their 20s (12 males with a mean age of 23.2 ± 1.7 and 5 females with a mean age of 21.0 ± 0.7) through participant recruitment announcements. Participants were required to have no hearing impairments or relevant medical history of brain disorders. Prior to the experiment, participants were advised to ensure sufficient sleep the night before, and they were instructed to refrain from behaviors such as smoking and drinking on the day of the experiment that could potentially affect fNIRS measurements. This study was approved by the Konkuk University Institutional Review Board (7001355-202105-HR-439). All methods were performed in accordance with the relevant guidelines and regulations by including a statement, and informed consent was obtained from all subjects. 2.2. Binaural beats (BB) To induce a 10 Hz Binaural Beats (BB) stimulation corresponding to the alpha wave, an auditory stimulator (Brand G, Model Q) was utilized. The left ear was presented with a frequency of 18000 Hz, while the right ear received a frequency of 18010 Hz. The experiment comprised three phases: Rest phase (5 min), Task phase (5 min), and another Rest phase (5 min). The Task phase included two conditions: "Task only," where participants performed the task without BB stimulation, and "Task + BB," where BB stimulation was presented concurrently with task performance (Fig. 1 ). All participants engaged in both task conditions, and the order was counterbalanced. 2.3. 3-back task In this study, we measured visuospatial memory using the 3-back task. Participants were instructed to press the space bar as quickly as possible if the currently presented image matched the one presented three times earlier. The images consisted of a white display in one of the four quadrants of a divided rectangle (Fig. 2 ). Each image was presented for 1 second, followed by a black screen with a white cross ("+") at the center during the 1-second interval between images. A total of 150 images, randomly selected from four categories, were presented, with 50 correct answers. To ensure smooth experiment execution, participants underwent sufficient practice trials before participating in the actual experiment. After completing all trials, Accuracy (%) and Reaction Time (ms) were calculated. To analyze the differences between the two conditions (Task only and Task + BB), a Paired t-test (SPSS 25, IBM, USA) was conducted. 2.4. Cerebral hemodynamics measurement & analysis We measured hemodynamic responses using fNIRS measurement system (NIRSport2®; NIRx Medical Technology, Berlin, Germany) with a sampling rate of 5.08 Hz. The system consists of sources emitting two wavelengths (760nm, 850nm) and 16 detectors each. To observe brain regions associated with visuospatial memory, optodes were attached to the Frontal, Temporal, Parietal, and Occipital areas according to the 10–20 system (sources: Fp1, Fp2, AFz, F1, F2, F5, F6, TP7, TP8, P1, P2, P5, P6, POz, O1, O2, detectors: Fpz, Fz, F3, F4, T7, T8, Pz, P3, P4, P7, P8, PO3, PO4, PO7, PO8, Oz), resulting in a total of 36 source-detector channels (Fig. 3 ). The distance between source-detector channels was set at 3.0 cm. The nirsLAB®software (v.2019.04; NIRx Medical Technology, Berlin, Germany) was utilized to transform optical data into hemodynamic data using the modified Beer-Lambert law. Initially, bandpass filtering from 0.01 to 0.2 Hz was applied to remove physiological noises (heartbeat, respiration, etc.). The data from phases other than the pre-task rest phase were normalized based on the rest phase data. The Differential Pathlength Factor (DPF) was set at 7.25 (Wavelength 1) and 6.38 (Wavelength 2), and oxyhemoglobin (HbO) concentrations were extracted. The extracted HbO concentrations in a time-series format were analyzed using MATLAB R2021b (Mathworks, USA). Paired t-tests (SPSS 25(IBM, USA)) were conducted to compare the average HbO concentrations across channels during the Task phase (5 min) between the two conditions. 3. Results 3.1. Task performance The results of the 3-back task are presented in Fig. 4 . The accuracy for the Task only condition was 66.8 ± 16.8%, and for the Task + BB condition, it was 68.2 ± 20.4%. The reaction time for the Task only condition was 753.2 ± 152.9 ms, while for the Task + BB condition, it was 699.4 ± 121.9 ms. Paired t-test results indicated a tendency for higher accuracy in the Task + BB condition compared to the Task only condition, although the difference was not statistically significant (p = 0.785). However, there was a significant reduction in reaction time in the Task + BB condition compared to the Task only condition (p = 0.046). 3.2. Cerebral hemodynamic responses The results of the HbO concentration comparison between the Task Only and Task + BB conditions are illustrated in Fig. 5(a). Significant differences were observed in three channels: F1-F3 (p = 0.010), F2-F4 (p = 0.043), and P2-P4 (p = 0.047). In these regions, the HbO concentration significantly increased in the Task + BB condition compared to the Task Only condition (Fig. 5(b)). 4. Discussion This study aimed to revisit the influence of inaudible Binaural Beats (BB) stimulation on visuospatial memory while exploring the direct impact of the induced brainwave changes on brain activation. Task performance metrics (Accuracy, Reaction time) and hemodynamic responses (HbO) were concurrently observed. Results indicated that, compared to the Task only condition where BB stimulation was not provided, the Task + BB condition exhibited a significant decrease in Reaction time and a trend of increased Accuracy during task execution. Analysis of hemodynamic responses revealed increased HbO concentrations in the F1-F3, F2-F4, and P2-P4 regions during the Task + BB condition. Thus, increased activation in specific brain regions during the Task + BB condition, compared to Task only, is anticipated to positively influence visuospatial memory. There have been reports suggesting that audible 10 Hz BB stimulation during Visual Reaction Time (VRT) tasks leads to shorter reaction times [ 14 ]. Furthermore, positive effects of BB in the alpha frequency band on cognitive abilities have been documented [ 15 – 19 ]. This study observed the positive impact of inaudible 10 Hz BB stimulation on visuospatial memory, reaffirming the pure effects of BB on cognition. Previous research on objectively elucidating the effects of Binaural Beats (BB) stimulation has predominantly focused on observing changes in brainwaves thought to be directly influenced by BB. However, studies employing methods such as functional Magnetic Resonance Imaging (fMRI) or fNIRS, allowing the observation of changes in brain activation associated with actual cognitive processing, are notably scarce. This study addresses this gap by utilizing fNIRS, which provides a convenient means to capture brain hemodynamic signals reflecting brain activation in a relatively unconstrained environment. The frontal lobe plays a crucial role in performing working memory tasks. Specifically, the Right Frontal lobe is reported to be activated during short-term memory tasks related to visuospatial information [ 20 ], while the Right Parietal lobe is activated during working memory tasks associated with visuospatial stimuli [ 21 ]. Therefore, the observed increase in activation in the F1-F3, F2-F4, and P2-P4 areas in this study is presumed to be closely related to the task, and the increased brain activation in these areas is expected to have a positive impact on task performance. Alpha waves, a type of brainwave emerging during states of rest before the onset of substantial brain activity, are considered absent when the mind is unable to relax, indicating tension or anxiety [ 22 ]. Moreover, alpha waves play a significant role in the working memory process [ 23 ], with reports suggesting an increase in alpha wave activity during the maintenance of working memory [ 24 – 26 ]. Although simultaneous measurement of brainwaves was not conducted in this study, the anticipated increase in alpha waves induced by BB stimulation suggests a positive impact on brain neural activity during task performance. In this study, we substantiate the favorable influence of inaudible frequency-range Binaural Beats (BB) stimulation on visuospatial memory by employing both behavioral data and the direct reflection of neural activation in cerebral hemodynamic responses. Although a direct comparison between brainwave signals and cerebral blood flow signals was not conducted, the significance of the findings is noteworthy. Furthermore, the limitation of exclusively utilizing participants in their twenties should be acknowledged. Future research endeavors should aim to address and broaden our understanding of the diverse aspects of the effects of BB stimulation by overcoming these limitations. Declarations Author Contribution Conceptualization, J.-S. K. and S.-C.C.; methodology, J.-S. K. and S.-C.C.; software, M.-H.C. and K.-B.K.; validation, J.-S.K. and S.-C.C.; formal analysis, H.-S.K.; investigation, K.-B.K. and Y.-B.J.; resources, H.-S.K.; data curation, Y.-B.J. and M.-K.L.; writing—original draft preparation, J.-S.K. and S.-C.C.; writing—review and editing, J.-S.K. and S.-C.C.; visualization, M.-H.C.; supervision, S.-C.C.; project administration, S.-C.C.; funding acquisition, H.-S.K. and S.-C.C. All authors have read and agreed to the published version of the manuscript. Acknowledgments This paper was supported by Konkuk University in 2023 Data Availability The datasets generated and/or analysed during the current study are not publicly available due [protection of personal biometric information] but are available from the corresponding author on reasonable request. References R. M. Ingendoh, E. S. Posny and A. Heine, Binaural beats to entrain the brain? 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Santed and J. M. Reales, Binaural auditory beats affect long-term memory, Psychol.Res. 83 (2019) 1124–1136. C. Beauchene, N. Abaid, R. Moran, R. A. Diana and A. Leonessa, The effect of binaural beats on verbal working memory and cortical connectivity, Journal of neural engineering 14 (2017) 026014. V. Prabhakaran, K. Narayanan, Z. Zhao and J. Gabrieli, Integration of diverse information in working memory within the frontal lobe, Nat.Neurosci. 3 (2000) 85–90. R. Bertaccini, G. Ellena, J. Macedo-Pascual, F. Carusi, J. Trajkovic, C. Poch and V. Romei, Parietal alpha oscillatory peak frequency mediates the effect of practice on visuospatial working memory performance, Vision 6 (2022) 30. J. Jeong and H. Kim, Assessment of the wear comfort of outdoorwear by ECG and EEG analyses, Journal of the Korean Society of Clothing and Textiles 33 (2009) 1665–1672. R. Wang, R. Kamezawa, A. Watanabe and K. Iramina, EEG alpha power change during working memory encoding in adults with different memory performance levels, (2017) 982–985. H. Van Dijk, I. L. Nieuwenhuis and O. Jensen, Left temporal alpha band activity increases during working memory retention of pitches, Eur.J.Neurosci. 31 (2010) 1701–1707. A. M. Tuladhar, N. t. Huurne, J. Schoffelen, E. Maris, R. Oostenveld and O. Jensen, Parieto-occipital sources account for the increase in alpha activity with working memory load, Hum.Brain Mapp. 28 (2007) 785–792. O. Jensen, J. Gelfand, J. Kounios and J. E. Lisman, Oscillations in the alpha band (9–12 Hz) increase with memory load during retention in a short-term memory task, Cerebral cortex 12 (2002) 877–882. Additional Declarations No competing interests reported. Cite Share Download PDF Status: Published Journal Publication published 16 Oct, 2024 Read the published version in Scientific Reports → Version 1 posted Editorial decision: Revision requested 29 Apr, 2024 Reviews received at journal 26 Apr, 2024 Reviewers agreed at journal 26 Apr, 2024 Reviews received at journal 22 Apr, 2024 Reviewers agreed at journal 22 Apr, 2024 Reviewers invited by journal 21 Apr, 2024 Editor assigned by journal 21 Apr, 2024 Editor invited by journal 11 Apr, 2024 Submission checks completed at journal 11 Apr, 2024 First submitted to journal 26 Mar, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4167182","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":291352880,"identity":"31ffa25e-1d2d-4d34-bcc0-3a15f575c53e","order_by":0,"name":"Ji-Su Kim","email":"","orcid":"","institution":"Konkuk University","correspondingAuthor":false,"prefix":"","firstName":"Ji-Su","middleName":"","lastName":"Kim","suffix":""},{"id":291352881,"identity":"afbde5bf-bb13-4098-b0e2-b00653c5eee4","order_by":1,"name":"Kyu-Beom Kim","email":"","orcid":"","institution":"Konkuk 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optodes.\u003c/p\u003e","description":"","filename":"floatimage3.png","url":"https://assets-eu.researchsquare.com/files/rs-4167182/v1/1c8638d5869a529ba54e20d1.png"},{"id":55004663,"identity":"83b8eb71-3e2d-4213-8432-197c9780ef13","added_by":"auto","created_at":"2024-04-19 18:47:01","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":67622,"visible":true,"origin":"","legend":"\u003cp\u003eThe 3-back task result according to the presence or absence of BB stimulation.\u003c/p\u003e","description":"","filename":"floatimage4.png","url":"https://assets-eu.researchsquare.com/files/rs-4167182/v1/32900a4c9316688cf75021e8.png"},{"id":55004667,"identity":"6625edc2-592f-4aa2-a84f-5cf013a63b37","added_by":"auto","created_at":"2024-04-19 18:47:02","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":89167,"visible":true,"origin":"","legend":"\u003cp\u003eCerebral hemodynamic responses\u003c/p\u003e","description":"","filename":"F5.png","url":"https://assets-eu.researchsquare.com/files/rs-4167182/v1/bdddcb5e248547e21d1ba99b.png"},{"id":67149154,"identity":"7b9eaca6-5e05-43fc-8f29-4491798c132d","added_by":"auto","created_at":"2024-10-21 16:12:28","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":726850,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4167182/v1/6d3b585c-9b6d-41e9-acfa-a665db2d403c.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"The Effects of Inaudible Binaural Beats on Visuospatial Memory: An fNIRS Study","fulltext":[{"header":"1. Introduction","content":"\u003cp\u003eBinaural Beats (BB) refer to auditory stimuli presented to both ears with different frequencies, inducing brainwave synchronization at the frequency difference [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. For example, presenting a 100 Hz base frequency to one ear and a BB stimulus with a base frequency plus a differential frequency of 110 Hz to the other ear would synchronize brainwaves at the differential frequency of 10 Hz [\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eNumerous studies have provided evidence supporting the positive effects of BB-induced brainwave entrainment on cognitive aspects [\u003cspan additionalcitationids=\"CR4\" citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. However, conflicting results suggesting no improvement in cognitive function due to BB stimulation have also been reported [\u003cspan additionalcitationids=\"CR7\" citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. The divergent outcomes in the effects of BB are expected to be attributed to various reasons, and one contributing factor could be the use of audible BB stimuli in previous studies, potentially impacting cognitive processing with sounds in the audible range [\u003cspan additionalcitationids=\"CR10\" citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eOur research team addressed this issue by eliminating the influence of audible sounds in prior studies and observed the brainwave entrainment effects of BB. Specifically, we validated the ability of inaudible BB with a base frequency of 18000 Hz and a differential frequency of 10 Hz to induce alpha waves [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]. Additionally, when evaluating visuospatial memory performance while presenting inaudible BB stimuli, we found an enhancement in task performance compared to conditions without stimulation, demonstrating the positive impact of pure BB stimuli on cognitive processing [\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eHowever, all previous studies, including our team's prior research, focused solely on observing changes in brainwaves based on rhythmic neural activity and did not directly observe brain activity. Therefore, studies directly observing the effects of BB on cognitive processes related to brain activation, such as changes in neural activity or cerebral blood flow, are currently lacking. To further validate the scientific impact of BB effects, additional research involving direct observation of brain neural activity is crucial.\u003c/p\u003e \u003cp\u003eHence, in this study, we aim to reexamine the impact of inaudible BB stimulation, free from the influence of sound, using a base frequency of 18000 Hz and a differential frequency of 10 Hz. Simultaneously, we seek to observe brain activation responses. We selected visuospatial memory, a representative cognitive task, and employed functional Near Infrared Spectroscopy (fNIRS), a convenient method for measuring brain hemodynamic responses closely associated with changes in brain activity.\u003c/p\u003e"},{"header":"2. Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003e2.1. Subjects\u003c/h2\u003e \u003cp\u003e We recruited a total of 17 healthy individuals in their 20s (12 males with a mean age of 23.2\u0026thinsp;\u0026plusmn;\u0026thinsp;1.7 and 5 females with a mean age of 21.0\u0026thinsp;\u0026plusmn;\u0026thinsp;0.7) through participant recruitment announcements. Participants were required to have no hearing impairments or relevant medical history of brain disorders. Prior to the experiment, participants were advised to ensure sufficient sleep the night before, and they were instructed to refrain from behaviors such as smoking and drinking on the day of the experiment that could potentially affect fNIRS measurements.\u003c/p\u003e \u003cp\u003e This study was approved by the Konkuk University Institutional Review Board (7001355-202105-HR-439). All methods were performed in accordance with the relevant guidelines and regulations by including a statement, and informed consent was obtained from all subjects.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003e2.2. Binaural beats (BB)\u003c/h2\u003e \u003cp\u003eTo induce a 10 Hz Binaural Beats (BB) stimulation corresponding to the alpha wave, an auditory stimulator (Brand G, Model Q) was utilized. The left ear was presented with a frequency of 18000 Hz, while the right ear received a frequency of 18010 Hz. The experiment comprised three phases: Rest phase (5 min), Task phase (5 min), and another Rest phase (5 min). The Task phase included two conditions: \"Task only,\" where participants performed the task without BB stimulation, and \"Task\u0026thinsp;+\u0026thinsp;BB,\" where BB stimulation was presented concurrently with task performance (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). All participants engaged in both task conditions, and the order was counterbalanced.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003e2.3. 3-back task\u003c/h2\u003e \u003cp\u003eIn this study, we measured visuospatial memory using the 3-back task. Participants were instructed to press the space bar as quickly as possible if the currently presented image matched the one presented three times earlier. The images consisted of a white display in one of the four quadrants of a divided rectangle (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). Each image was presented for 1 second, followed by a black screen with a white cross (\"+\") at the center during the 1-second interval between images. A total of 150 images, randomly selected from four categories, were presented, with 50 correct answers. To ensure smooth experiment execution, participants underwent sufficient practice trials before participating in the actual experiment. After completing all trials, Accuracy (%) and Reaction Time (ms) were calculated. To analyze the differences between the two conditions (Task only and Task\u0026thinsp;+\u0026thinsp;BB), a Paired t-test (SPSS 25, IBM, USA) was conducted.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003e2.4. Cerebral hemodynamics measurement \u0026amp; analysis\u003c/h2\u003e \u003cp\u003eWe measured hemodynamic responses using fNIRS measurement system (NIRSport2\u0026reg;; NIRx Medical Technology, Berlin, Germany) with a sampling rate of 5.08 Hz. The system consists of sources emitting two wavelengths (760nm, 850nm) and 16 detectors each. To observe brain regions associated with visuospatial memory, optodes were attached to the Frontal, Temporal, Parietal, and Occipital areas according to the 10\u0026ndash;20 system (sources: Fp1, Fp2, AFz, F1, F2, F5, F6, TP7, TP8, P1, P2, P5, P6, POz, O1, O2, detectors: Fpz, Fz, F3, F4, T7, T8, Pz, P3, P4, P7, P8, PO3, PO4, PO7, PO8, Oz), resulting in a total of 36 source-detector channels (Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). The distance between source-detector channels was set at 3.0 cm.\u003c/p\u003e \u003cp\u003eThe nirsLAB\u0026reg;software (v.2019.04; NIRx Medical Technology, Berlin, Germany) was utilized to transform optical data into hemodynamic data using the modified Beer-Lambert law. Initially, bandpass filtering from 0.01 to 0.2 Hz was applied to remove physiological noises (heartbeat, respiration, etc.). The data from phases other than the pre-task rest phase were normalized based on the rest phase data. The Differential Pathlength Factor (DPF) was set at 7.25 (Wavelength 1) and 6.38 (Wavelength 2), and oxyhemoglobin (HbO) concentrations were extracted.\u003c/p\u003e \u003cp\u003eThe extracted HbO concentrations in a time-series format were analyzed using MATLAB R2021b (Mathworks, USA). Paired t-tests (SPSS 25(IBM, USA)) were conducted to compare the average HbO concentrations across channels during the Task phase (5 min) between the two conditions.\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e"},{"header":"3. Results","content":"\u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003e3.1. Task performance\u003c/h2\u003e \u003cp\u003eThe results of the 3-back task are presented in Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e. The accuracy for the Task only condition was 66.8\u0026thinsp;\u0026plusmn;\u0026thinsp;16.8%, and for the Task\u0026thinsp;+\u0026thinsp;BB condition, it was 68.2\u0026thinsp;\u0026plusmn;\u0026thinsp;20.4%. The reaction time for the Task only condition was 753.2\u0026thinsp;\u0026plusmn;\u0026thinsp;152.9 ms, while for the Task\u0026thinsp;+\u0026thinsp;BB condition, it was 699.4\u0026thinsp;\u0026plusmn;\u0026thinsp;121.9 ms. Paired t-test results indicated a tendency for higher accuracy in the Task\u0026thinsp;+\u0026thinsp;BB condition compared to the Task only condition, although the difference was not statistically significant (p\u0026thinsp;=\u0026thinsp;0.785). However, there was a significant reduction in reaction time in the Task\u0026thinsp;+\u0026thinsp;BB condition compared to the Task only condition (p\u0026thinsp;=\u0026thinsp;0.046).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003e3.2. Cerebral hemodynamic responses\u003c/h2\u003e \u003cp\u003eThe results of the HbO concentration comparison between the Task Only and Task\u0026thinsp;+\u0026thinsp;BB conditions are illustrated in Fig.\u0026nbsp;5(a). Significant differences were observed in three channels: F1-F3 (p\u0026thinsp;=\u0026thinsp;0.010), F2-F4 (p\u0026thinsp;=\u0026thinsp;0.043), and P2-P4 (p\u0026thinsp;=\u0026thinsp;0.047). In these regions, the HbO concentration significantly increased in the Task\u0026thinsp;+\u0026thinsp;BB condition compared to the Task Only condition (Fig.\u0026nbsp;5(b)).\u003c/p\u003e\u003c/div\u003e"},{"header":"4. Discussion","content":"\u003cp\u003eThis study aimed to revisit the influence of inaudible Binaural Beats (BB) stimulation on visuospatial memory while exploring the direct impact of the induced brainwave changes on brain activation. Task performance metrics (Accuracy, Reaction time) and hemodynamic responses (HbO) were concurrently observed.\u003c/p\u003e \u003cp\u003e Results indicated that, compared to the Task only condition where BB stimulation was not provided, the Task\u0026thinsp;+\u0026thinsp;BB condition exhibited a significant decrease in Reaction time and a trend of increased Accuracy during task execution. Analysis of hemodynamic responses revealed increased HbO concentrations in the F1-F3, F2-F4, and P2-P4 regions during the Task\u0026thinsp;+\u0026thinsp;BB condition. Thus, increased activation in specific brain regions during the Task\u0026thinsp;+\u0026thinsp;BB condition, compared to Task only, is anticipated to positively influence visuospatial memory.\u003c/p\u003e \u003cp\u003eThere have been reports suggesting that audible 10 Hz BB stimulation during Visual Reaction Time (VRT) tasks leads to shorter reaction times [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e]. Furthermore, positive effects of BB in the alpha frequency band on cognitive abilities have been documented [\u003cspan additionalcitationids=\"CR16 CR17 CR18\" citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e]. This study observed the positive impact of inaudible 10 Hz BB stimulation on visuospatial memory, reaffirming the pure effects of BB on cognition.\u003c/p\u003e \u003cp\u003ePrevious research on objectively elucidating the effects of Binaural Beats (BB) stimulation has predominantly focused on observing changes in brainwaves thought to be directly influenced by BB. However, studies employing methods such as functional Magnetic Resonance Imaging (fMRI) or fNIRS, allowing the observation of changes in brain activation associated with actual cognitive processing, are notably scarce. This study addresses this gap by utilizing fNIRS, which provides a convenient means to capture brain hemodynamic signals reflecting brain activation in a relatively unconstrained environment. The frontal lobe plays a crucial role in performing working memory tasks. Specifically, the Right Frontal lobe is reported to be activated during short-term memory tasks related to visuospatial information [\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e], while the Right Parietal lobe is activated during working memory tasks associated with visuospatial stimuli [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e]. Therefore, the observed increase in activation in the F1-F3, F2-F4, and P2-P4 areas in this study is presumed to be closely related to the task, and the increased brain activation in these areas is expected to have a positive impact on task performance.\u003c/p\u003e \u003cp\u003eAlpha waves, a type of brainwave emerging during states of rest before the onset of substantial brain activity, are considered absent when the mind is unable to relax, indicating tension or anxiety [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e]. Moreover, alpha waves play a significant role in the working memory process [\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e], with reports suggesting an increase in alpha wave activity during the maintenance of working memory [\u003cspan additionalcitationids=\"CR25\" citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e]. Although simultaneous measurement of brainwaves was not conducted in this study, the anticipated increase in alpha waves induced by BB stimulation suggests a positive impact on brain neural activity during task performance.\u003c/p\u003e \u003cp\u003eIn this study, we substantiate the favorable influence of inaudible frequency-range Binaural Beats (BB) stimulation on visuospatial memory by employing both behavioral data and the direct reflection of neural activation in cerebral hemodynamic responses. Although a direct comparison between brainwave signals and cerebral blood flow signals was not conducted, the significance of the findings is noteworthy. Furthermore, the limitation of exclusively utilizing participants in their twenties should be acknowledged. Future research endeavors should aim to address and broaden our understanding of the diverse aspects of the effects of BB stimulation by overcoming these limitations.\u003c/p\u003e"},{"header":"Declarations","content":"\u003ch2\u003eAuthor Contribution\u003c/h2\u003e\u003cp\u003eConceptualization, J.-S. K. and S.-C.C.; methodology, J.-S. K. and S.-C.C.; software, M.-H.C. and K.-B.K.; validation, J.-S.K. and S.-C.C.; formal analysis, H.-S.K.; investigation, K.-B.K. and Y.-B.J.; resources, H.-S.K.; data curation, Y.-B.J. and M.-K.L.; writing\u0026mdash;original draft preparation, J.-S.K. and S.-C.C.; writing\u0026mdash;review and editing, J.-S.K. and S.-C.C.; visualization, M.-H.C.; supervision, S.-C.C.; project administration, S.-C.C.; funding acquisition, H.-S.K. and S.-C.C. All authors have read and agreed to the published version of the manuscript.\u003c/p\u003e\u003ch2\u003eAcknowledgments\u003c/h2\u003e \u003cp\u003eThis paper was supported by Konkuk University in 2023\u003c/p\u003e\u003ch2\u003eData Availability\u003c/h2\u003e\u003cp\u003eThe datasets generated and/or analysed during the current study are not publicly available due [protection of personal biometric information] but are available from the corresponding author on reasonable request.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eR. M. Ingendoh, E. S. Posny and A. Heine, Binaural beats to entrain the brain? A systematic review of the effects of binaural beat stimulation on brain oscillatory activity, and the implications for psychological research and intervention, Plos one 18 (2023) e0286023.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eC. Kasprzak, Influence of binaural beats on EEG signal, Acta physica polonica A 119 (2011) 986\u0026ndash;990.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eN. Jirakittayakorn and Y. Wongsawat, Brain responses to a 6-Hz binaural beat: effects on general theta rhythm and frontal midline theta activity, Frontiers in neuroscience 11 (2017) 365.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eN. M. Puzi, R. Jailani, H. Norhazman and N. M. Zaini, Alpha and Beta brainwave characteristics to binaural beat treatment, (2013) 344\u0026ndash;348.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJ. Park, H. Kwon, S. Kang and Y. Lee, The effect of binaural beat-based audiovisual stimulation on brain waves and concentration, (2018) 420\u0026ndash;423.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eC. Beauchene, N. Abaid, R. Moran, R. A. Diana and A. Leonessa, The effect of binaural beats on visuospatial working memory and cortical connectivity, PloS one 11 (2016) e0166630.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eV. Rakhshan, P. Hassani-Abharian, M. Joghataei, M. Nasehi and R. Khosrowabadi, Effects of the Alpha, Beta, and Gamma Binaural Beat Brain Stimulation and Short-Term Training on Simultaneously Assessed Visuospatial and Verbal Working Memories, Signal Detection Measures, Response Times, and Intrasubject Response Time Variabilities: A Within-Subject Randomized Placebo-Controlled Clinical Trial, BioMed Research International 2022 (2022)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eA. Crespo, M. Recuero, G. Galvez and A. Bego\u0026ntilde;a, Effect of binaural stimulation on attention and EEG, Archives of Acoustics 38 (2013) 517\u0026ndash;528.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eM. Georgescu, D. Georgescu, M. Iancau and A. Gadidov, Effects of monotonous auditory stimulation on the human EEG, Neuroscience and Medicine 3 (2012) 337\u0026ndash;343.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJ. C. McLachlan, Music and spatial task performance, Nature 366 (1993) 520.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eF. H. Rauscher, G. L. Shaw and K. N. Ky, Listening to Mozart enhances spatial-temporal reasoning: towards a neurophysiological basis, Neurosci.Lett. 185 (1995) 44\u0026ndash;47.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eM. Choi, J. Jung, K. Kim, Y. Kim, J. Lee, H. Kim, J. Yi, O. Kang, Y. Kang and S. Chung, Effect of binaural beat in the inaudible band on EEG (STROBE), Medicine 101 (2022)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eY. Kim, K. Kim, J. Kim, H. Kim, M. Choi, J. Yi and S. Chung, Effects of inaudible binaural beats on visuospatial memory, Neuroreport 34 (2023) 501\u0026ndash;505.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eL. Shekar, C. A. Suryavanshi and K. R. Nayak, Effect of alpha and gamma binaural beats on reaction time and short-term memory, National Journal of Physiology, Pharmacy and Pharmacology 8 (2018) 829\u0026ndash;833.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJ. L. Carter and H. L. Russell, A pilot investigation of auditory and visual entrainment of brain wave activity in learning disabled boys, Texas Researcher 4 (1993) 65\u0026ndash;75.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJ. Kraus and M. Porubanov\u0026aacute;, The effect of binaural beats on working memory capacity, Studia psychologica 57 (2015) 135.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eM. D. Mujib, M. A. Hasan, S. A. Qazi and A. Vuckovic, Understanding the neurological mechanism involved in enhanced memory recall task following binaural beat: a pilot study, Experimental Brain Research 239 (2021) 2741\u0026ndash;2754.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eM. Garcia-Argibay, M. A. Santed and J. M. Reales, Binaural auditory beats affect long-term memory, Psychol.Res. 83 (2019) 1124\u0026ndash;1136.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eC. Beauchene, N. Abaid, R. Moran, R. A. Diana and A. Leonessa, The effect of binaural beats on verbal working memory and cortical connectivity, Journal of neural engineering 14 (2017) 026014.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eV. Prabhakaran, K. Narayanan, Z. Zhao and J. Gabrieli, Integration of diverse information in working memory within the frontal lobe, Nat.Neurosci. 3 (2000) 85\u0026ndash;90.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eR. Bertaccini, G. Ellena, J. Macedo-Pascual, F. Carusi, J. Trajkovic, C. Poch and V. Romei, Parietal alpha oscillatory peak frequency mediates the effect of practice on visuospatial working memory performance, Vision 6 (2022) 30.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJ. Jeong and H. Kim, Assessment of the wear comfort of outdoorwear by ECG and EEG analyses, Journal of the Korean Society of Clothing and Textiles 33 (2009) 1665\u0026ndash;1672.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eR. Wang, R. Kamezawa, A. Watanabe and K. Iramina, EEG alpha power change during working memory encoding in adults with different memory performance levels, (2017) 982\u0026ndash;985.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eH. Van Dijk, I. L. Nieuwenhuis and O. Jensen, Left temporal alpha band activity increases during working memory retention of pitches, Eur.J.Neurosci. 31 (2010) 1701\u0026ndash;1707.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eA. M. Tuladhar, N. t. Huurne, J. Schoffelen, E. Maris, R. Oostenveld and O. Jensen, Parieto-occipital sources account for the increase in alpha activity with working memory load, Hum.Brain Mapp. 28 (2007) 785\u0026ndash;792.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eO. Jensen, J. Gelfand, J. Kounios and J. E. Lisman, Oscillations in the alpha band (9\u0026ndash;12 Hz) increase with memory load during retention in a short-term memory task, Cerebral cortex 12 (2002) 877\u0026ndash;882.\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Binaural Beats, fNIRS, cerebral hemodynamic, visuospatial memory","lastPublishedDoi":"10.21203/rs.3.rs-4167182/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4167182/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThis study aimed to observe the impact of pure Binaural Beats (BB) stimulation in the inaudible frequency range, excluding the influence of sound, on visuospatial memory. Additionally, we investigated whether the brainwave changes induced by BB stimulation directly affect brain activation. The experiment involved 17 participants (12 males with a mean age of 23.2\u0026thinsp;\u0026plusmn;\u0026thinsp;1.7 and 5 females with a mean age of 21.0\u0026thinsp;\u0026plusmn;\u0026thinsp;0.7) in their 20s. Each participant received 10 Hz BB stimulation by presenting frequencies of 18000 Hz and 18010 Hz to the left and right ears, respectively. The experiment consisted of Rest phase (5min), Task phase (5min), and Rest phase (5min). The Task phase included conditions where participants performed the task either without BB stimulation \"Task only\" or with BB stimulation \"Task\u0026thinsp;+\u0026thinsp;BB\". Visuospatial memory was evaluated using the 3-back task. To observe brain activation, functional Near Infrared Spectroscopy (fNIRS) was employed to measure hemodynamic responses in all phases. The cognitive task performance (Accuracy, Reaction time) and oxyhemoglobin (HbO) concentration during the Task phase were compared between conditions with and without BB stimulation using paired t-tests. Results indicated a significantly shorter Reaction time in the Task\u0026thinsp;+\u0026thinsp;BB condition compared to the Task only condition. Moreover, an increase in HbO concentration was observed in the F1-F3, F2-F4, and P2-P4 regions during the Task\u0026thinsp;+\u0026thinsp;BB condition. In conclusion, the observed increase in HbO concentration suggests a positive influence on task performance. This study is meaningful in objectively demonstrating the impact of inaudible BB stimulation on visuospatial memory, utilizing both behavioral data and direct neural activation reflected in hemodynamic responses.\u003c/p\u003e","manuscriptTitle":"The Effects of Inaudible Binaural Beats on Visuospatial Memory: An fNIRS Study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-04-19 18:46:55","doi":"10.21203/rs.3.rs-4167182/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2024-04-29T07:50:00+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-04-26T12:18:08+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"4e69b0c4-5d1f-4ac3-bc7a-0191434abc24","date":"2024-04-26T11:48:41+00:00","index":"hide","fulltext":""},{"type":"editorInvitedReview","content":"","date":"2024-04-22T10:20:06+00:00","index":"hide","fulltext":""},{"type":"reviewerAgreed","content":"3824ff99-0d77-4c6f-8324-d285e8f456e3","date":"2024-04-22T09:40:08+00:00","index":"hide","fulltext":""},{"type":"reviewersInvited","content":"","date":"2024-04-21T11:22:17+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-04-21T04:47:10+00:00","index":"","fulltext":""},{"type":"editorInvited","content":"","date":"2024-04-11T11:43:50+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-04-11T11:43:00+00:00","index":"","fulltext":""},{"type":"submitted","content":"Scientific Reports","date":"2024-03-26T05:41:49+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"scientific-reports","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"scirep","sideBox":"Learn more about [Scientific Reports](http://www.nature.com/srep/)","snPcode":"","submissionUrl":"","title":"Scientific Reports","twitterHandle":"","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"stoa","reportingPortfolio":"Scientific Reports","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"157aefe8-d508-4640-9592-60a833b1bfef","owner":[],"postedDate":"April 19th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[{"id":30689050,"name":"Biological sciences/Neuroscience"},{"id":30689051,"name":"Health sciences/Health care"}],"tags":[],"updatedAt":"2024-10-21T16:06:01+00:00","versionOfRecord":{"articleIdentity":"rs-4167182","link":"https://doi.org/10.1038/s41598-024-74784-9","journal":{"identity":"scientific-reports","isVorOnly":false,"title":"Scientific Reports"},"publishedOn":"2024-10-16 15:57:05","publishedOnDateReadable":"October 16th, 2024"},"versionCreatedAt":"2024-04-19 18:46:55","video":"","vorDoi":"10.1038/s41598-024-74784-9","vorDoiUrl":"https://doi.org/10.1038/s41598-024-74784-9","workflowStages":[]},"version":"v1","identity":"rs-4167182","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4167182","identity":"rs-4167182","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}