Modulation of Item and Source Memory by Auditory Beat Stimulation: A Pilot Study With Intracranial EEG

Auditory beat stimulation is an upcoming technique for non-invasive brain stimulation. Its influence on mediotemporal regions and memory processes has not yet been thoroughly investigated. A recent study suggests that auditory beats are able to alter intracranial EEG (iEEG) power and phase synchronization. 5 Hz binaural beat stimulation increased temporo-lateral phase synchronization, while 5 Hz monaural beat stimulation decreased mediotemporal synchronization. Based on the relevance of phase synchronization for memory operations, we hypothesized that 5 Hz binaural beat stimulation enhances, while 5 Hz monaural beat stimulation decreases long-term memory performance. We analyzed data from presurgical epilepsy patients with implanted depth electrodes in the hippocampus and rhinal cortex. 5 Hz monaural and binaural beat vs. control stimulation was applied while patients performed an associative learning task involving item and source recognition. We evaluated behavioral effects for item (hits minus false alarms) and source memory (correct minus incorrect) and the impact of auditory beats on iEEG power, rhinal-hippocampal phase synchronization and inter-trial phase locking. A three-way repeated measures ANOVA (encoding/retrieval, item/source, monaural/binaural/control) revealed a main effect of stimulation (p = 0.03) and a linear effect in the expected direction: binaural > control > monaural (p = 0.036). Both monaural and binaural stimulation were associated with increased phase locking of 5 Hz oscillations within rhinal cortex. These phase locking increases, however, corresponded to reverse phase shifts. Our data suggest that binaural vs. monaural 5 Hz stimulation increases vs. decreases long-term memory performance. These behavioral effects appear to be related to reverse phase shifts within rhinal cortex.

[1]  Sean M Montgomery,et al.  The Effect of Spatially Inhomogeneous Extracellular Electric Fields on Neurons , 2010, The Journal of Neuroscience.

[2]  Dong Ming,et al.  Analysis of EEG activity in response to binaural beats with different frequencies. , 2014, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[3]  R. Henson,et al.  Memory signals are temporally dissociated within and across human hippocampus and perirhinal cortex , 2012, Nature Neuroscience.

[4]  B. N'Kaoua,et al.  Intracranial topography of event-related potentials (N400/P600) elicited during a continuous recognition memory task. , 1995, Psychophysiology.

[5]  Nikolai Axmacher,et al.  Using state-trace analysis to dissociate the functions of the human hippocampus and perirhinal cortex in recognition memory , 2013, Proceedings of the National Academy of Sciences.

[6]  B. Ross,et al.  Human cortical responses to slow and fast binaural beats reveal multiple mechanisms of binaural hearing. , 2014, Journal of neurophysiology.

[7]  Lila Davachi,et al.  Selective and Shared Contributions of the Hippocampus and Perirhinal Cortex to Episodic Item and Associative Encoding , 2008, Journal of Cognitive Neuroscience.

[8]  Philipp Berens,et al.  CircStat: AMATLABToolbox for Circular Statistics , 2009, Journal of Statistical Software.

[9]  Suhasa B. Kodandaramaiah,et al.  Noninvasive Deep Brain Stimulation via Temporally Interfering Electric Fields , 2017, Cell.

[10]  Binaural beat salience , 2012, Hearing Research.

[11]  Diane M. Beck,et al.  To See or Not to See: Prestimulus α Phase Predicts Visual Awareness , 2009, The Journal of Neuroscience.

[12]  C. Bauckhage,et al.  Prediction of memory formation based on absolute electroencephalographic phases in rhinal cortex and hippocampus outperforms prediction based on stimulus‐related phase shifts , 2018, The European journal of neuroscience.

[13]  L. Colgin.  Mechanisms and functions of theta rhythms. , 2013, Annual review of neuroscience.

[14]  R. VanRullen,et al.  The Phase of Ongoing EEG Oscillations Predicts Visual Perception , 2009, The Journal of Neuroscience.

[15]  P. Campo,et al.  Impact of auditory stimulation at a frequency of 5 Hz in verbal memory. , 2008, Actas espanolas de psiquiatria.

[16]  M. Nitsche,et al.  Studying and modifying brain function with non-invasive brain stimulation , 2018, Nature Neuroscience.

[17]  B. Hommel,et al.  High-Frequency Binaural Beats Increase Cognitive Flexibility: Evidence from Dual-Task Crosstalk , 2016, Front. Psychol..

[18]  Timm Rosburg,et al.  Intracranially Recorded Memory-related Potentials Reveal Higher Posterior than Anterior Hippocampal Involvement in Verbal Encoding and Retrieval , 2008, Journal of Cognitive Neuroscience.

[19]  Christian Bauckhage,et al.  Prediction of successful memory encoding based on single-trial rhinal and hippocampal phase information , 2016, NeuroImage.

[20]  D. Schwarz,et al.  Human auditory steady state responses to binaural and monaural beats , 2005, Clinical Neurophysiology.

[21]  D. Wozniak,et al.  Ataxia and Paroxysmal Dyskinesia in Mice Lacking Axonally Transported FGF14 , 2002, Neuron.

[22]  Beth A. Lopour,et al.  Coding of Information in the Phase of Local Field Potentials within Human Medial Temporal Lobe , 2013, Neuron.

[23]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[24]  N. Axmacher,et al.  Electrical engram: how deep brain stimulation affects memory , 2013, Trends in Cognitive Sciences.

[25]  K Lehnertz,et al.  Evidence relating human verbal memory to hippocampal N-methyl-D-aspartate receptors. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Helané Wahbeh,et al.  Binaural beat technology in humans: a pilot study to assess neuropsychologic, physiologic, and electroencephalographic effects. , 2007, Journal of alternative and complementary medicine.

[27]  J. Reales,et al.  Efficacy of binaural auditory beats in cognition, anxiety, and pain perception: a meta-analysis , 2018, Psychological Research.

[28]  Nikolai Axmacher,et al.  Intracranial electroencephalography power and phase synchronization changes during monaural and binaural beat stimulation , 2015, The European journal of neuroscience.

[29]  Thomas Elbert,et al.  Threshold regulation - a key to the understanding of the combined dynamics of EEG and event-related potentials , 1987 .

[30]  Y. Yamaguchi,et al.  A unified view of theta-phase coding in the entorhinal–hippocampal system , 2007, Current Opinion in Neurobiology.

[31]  W. Singer,et al.  Modulation of Neuronal Interactions Through Neuronal Synchronization , 2007, Science.

[32]  G. McCarthy,et al.  Language-related field potentials in the anterior-medial temporal lobe: II. Effects of word type and semantic priming , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[33]  N. Erbil,et al.  Lateralisation of sound in temporal-lobe epilepsy: Comparison between pre- and postoperative performances and ERPs , 2012, Clinical Neurophysiology.

[34]  Carsten H. Wolters,et al.  Good vibrations: Oscillatory phase shapes perception , 2012, NeuroImage.

[35]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[36]  Sang Ah Lee,et al.  Direct Electrical Stimulation of the Human Entorhinal Region and Hippocampus Impairs Memory , 2016, Neuron.

[37]  T. Picton,et al.  Human auditory steady-state responses: Respuestas auditivas de estado estable en humanos , 2003, International journal of audiology.

[38]  X.L. Chen,et al.  Deep Brain Stimulation , 2013, Interventional Neurology.

[39]  José M. Reales,et al.  Binaural auditory beats affect long-term memory , 2019, Psychological research.

[40]  D. McCormick,et al.  Endogenous Electric Fields May Guide Neocortical Network Activity , 2010, Neuron.

[41]  A. Starr,et al.  Binaural interaction in the superior olivary complex of the cat: an analysis of field potentials evoked by binaural-beat stimuli. , 1968, Journal of neurophysiology.

[42]  B. Winblad,et al.  The Magnitude of Dementia Occurrence in the World , 2003, Alzheimer disease and associated disorders.

[43]  Nir Lipsman,et al.  Deep Brain Stimulation for Disorders of Memory and Cognition , 2014, Neurotherapeutics.

[44]  Job P. Lindsen,et al.  Electrical Brain Responses to an Auditory Illusion and the Impact of Musical Expertise , 2015, PloS one.

[45]  Juergen Fell,et al.  Auditory Beat Stimulation and its Effects on Cognition and Mood States , 2015, Front. Psychiatry.

[46]  D. Blum.  The Human Hippocampus , 1989, Neurology.

[47]  I. Fried,et al.  Memory enhancement and deep-brain stimulation of the entorhinal area. , 2012, The New England journal of medicine.

[48]  S. Tillery,et al.  Transcranial Pulsed Ultrasound Stimulates Intact Brain Circuits , 2010, Neuron.

[49]  J. Fell,et al.  The role of phase synchronization in memory processes , 2011, Nature Reviews Neuroscience.

[50]  C. C. Wood,et al.  Potentials evoked in human and monkey medial temporal lobe during auditory and visual oddball paradigms. , 1992, Electroencephalography and clinical neurophysiology.

[51]  Xiao-Hua Zhou,et al.  Statistical Methods for Meta‐Analysis , 2008 .

[52]  B. Staresina,et al.  Memory encoding‐related anterior hippocampal potentials are modulated by deep brain stimulation of the entorhinal area , 2018, Hippocampus.

[53]  Nikolai Axmacher,et al.  Phase-locking within human mediotemporal lobe predicts memory formation , 2008, NeuroImage.

[54]  J. Fell,et al.  The Impact of Monaural Beat Stimulation on Anxiety and Cognition , 2017, Front. Hum. Neurosci..