Brain Network Activation (BNA) Reveals Scopolamine-induced Impairment of Visual Working Memory

Overview

Journal J Mol Neurosci

Specialties Molecular Biology
Neurology

Date 2014 Feb 19

PMID 24535560

Citations 8

Authors

Amit Reches

Naama Levy-Cooperman

Ilan Laufer

Revital Shani-Hershkovitch

Keren Ziv

Dani Kerem

Noga Gal

Yaki Stern

Guy Cukierman

Myroslava K Romach

Edward M Sellers

Amir B Geva

Affiliations

Soon will be listed here.

Abstract

The overarching goal of this event-related potential (ERP) study was to examine the effects of scopolamine on the dynamics of brain network activation using a novel ERP network analysis method known as Brain Network Activation (BNA). BNA was used for extracting group-common stimulus-activated network patterns elicited to matching probe stimuli in the context of a delayed matching-to-sample task following placebo and scopolamine treatments administered to healthy participants. The BNA extracted networks revealed the existence of two pathophysiological mechanisms following scopolamine, disconnection, and compensation. Specifically, weaker frontal theta and parietal alpha coupling was accompanied with enhanced fronto-centro-parietal theta activation relative to placebo. In addition, using the characteristic BNA network of each treatment as well as corresponding literature-guided selective subnetworks as combined biomarkers managed to differentiate between individual responses to each of the treatments. Behavioral effects associated with scopolamine included delayed response time and impaired response accuracy. These results indicate that the BNA method is sensitive to the effects of scopolamine on working memory and that it may potentially enable diagnosis and treatment assessment of dysfunctions associated with cholinergic deficiency.

Citing Articles

Brain Network Analysis of EEG Recordings Can Be Used to Assess Cognitive Function in Teenagers With 15q13.3 Microdeletion Syndrome.

Stern T, Crutcher E, McCarthy J, Ali M, Issachar G, Geva A Front Neurosci. 2021; 15:622329.

PMID: 33584189 PMC: 7876406. DOI: 10.3389/fnins.2021.622329.

No Seasonal Changes in Cognitive Functioning Among High School Football Athletes: Implementation of a Novel Electrophysiological Measure and Standard Clinical Measures.

Broglio S, Williams R, Rettmann A, Moore B, Eckner J, Meehan S Clin J Sport Med. 2017; 28(2):130-138.

PMID: 28727640 PMC: 5767537. DOI: 10.1097/JSM.0000000000000420.

Preliminary investigation of Brain Network Activation (BNA) and its clinical utility in sport-related concussion.

Reches A, Kutcher J, Elbin R, Or-Ly H, Sadeh B, Greer J Brain Inj. 2017; 31(2):237-246.

PMID: 28055228 PMC: 5351793. DOI: 10.1080/02699052.2016.1231343.

Investigating a Novel Measure of Brain Networking Following Sports Concussion.

Broglio S, Rettmann A, Greer J, Brimacombe S, Moore B, Narisetty N Int J Sports Med. 2016; 37(9):714-22.

PMID: 27286176 PMC: 4972660. DOI: 10.1055/s-0042-107250.

Stability of an ERP-based measure of brain network activation (BNA) in athletes: A new electrophysiological assessment tool for concussion.

Eckner J, Rettmann A, Narisetty N, Greer J, Moore B, Brimacombe S Brain Inj. 2016; 30(9):1075-81.

PMID: 27245767 PMC: 4988883. DOI: 10.3109/02699052.2016.1160152.

References

Onton J, Delorme A, Makeig S . Frontal midline EEG dynamics during working memory. Neuroimage. 2005; 27(2):341-56. DOI: 10.1016/j.neuroimage.2005.04.014. View

Miller B, Deouell L, Dam C, Knight R, DEsposito M . Spatio-temporal dynamics of neural mechanisms underlying component operations in working memory. Brain Res. 2008; 1206:61-75. PMC: 4026171. DOI: 10.1016/j.brainres.2008.01.059. View

Shahaf G, Reches A, Pinchuk N, Fisher T, Ben Bashat G, Kanter A . Introducing a novel approach of network oriented analysis of ERPs, demonstrated on adult attention deficit hyperactivity disorder. Clin Neurophysiol. 2012; 123(8):1568-80. DOI: 10.1016/j.clinph.2011.12.010. View

Sauseng P, Klimesch W, Gruber W, Doppelmayr M, Stadler W, Schabus M . The interplay between theta and alpha oscillations in the human electroencephalogram reflects the transfer of information between memory systems. Neurosci Lett. 2002; 324(2):121-4. DOI: 10.1016/s0304-3940(02)00225-2. View

Plakke B, Ng C, Poremba A . Scopolamine impairs auditory delayed matching-to-sample performance in monkeys. Neurosci Lett. 2008; 438(1):126-30. PMC: 2696804. DOI: 10.1016/j.neulet.2008.04.015. View

Furey M, Pietrini P, Haxby J . Cholinergic enhancement and increased selectivity of perceptual processing during working memory. Science. 2000; 290(5500):2315-9. DOI: 10.1126/science.290.5500.2315. View

Ioannides A, Dimitriadis S, Saridis G, Voultsidou M, Poghosyan V, Liu L . Source space analysis of event-related dynamic reorganization of brain networks. Comput Math Methods Med. 2012; 2012:452503. PMC: 3477559. DOI: 10.1155/2012/452503. View

Araujo J, Chan A, Winka L, Seymour P, Milgram N . Dose-specific effects of scopolamine on canine cognition: impairment of visuospatial memory, but not visuospatial discrimination. Psychopharmacology (Berl). 2004; 175(1):92-8. DOI: 10.1007/s00213-004-1777-y. View

POTTER D, Pickles C, Roberts R, Rugg M . Scopolamine impairs memory performance and reduces frontal but not parietal visual P3 amplitude. Biol Psychol. 2000; 52(1):37-52. DOI: 10.1016/s0301-0511(99)00023-x. View

10.

Banko E, Vidnyanszky Z . Retention interval affects visual short-term memory encoding. J Neurophysiol. 2010; 103(3):1425-30. DOI: 10.1152/jn.00868.2009. View

11.

Shapiro A, Benedict R, Schretlen D, Brandt J . Construct and concurrent validity of the Hopkins Verbal Learning Test-revised. Clin Neuropsychol. 2000; 13(3):348-58. DOI: 10.1076/clin.13.3.348.1749. View

12.

Bentin S, Allison T, Puce A, Perez E, McCarthy G . Electrophysiological Studies of Face Perception in Humans. J Cogn Neurosci. 2010; 8(6):551-565. PMC: 2927138. DOI: 10.1162/jocn.1996.8.6.551. View

13.

Ebert U, Kirch W . Scopolamine model of dementia: electroencephalogram findings and cognitive performance. Eur J Clin Invest. 1998; 28(11):944-9. DOI: 10.1046/j.1365-2362.1998.00393.x. View

14.

Buccafusco J, Terry Jr A, Webster S, Martin D, Hohnadel E, Bouchard K . The scopolamine-reversal paradigm in rats and monkeys: the importance of computer-assisted operant-conditioning memory tasks for screening drug candidates. Psychopharmacology (Berl). 2007; 199(3):481-94. DOI: 10.1007/s00213-007-0887-8. View

15.

Grady C, Furey M, Pietrini P, Horwitz B, Rapoport S . Altered brain functional connectivity and impaired short-term memory in Alzheimer's disease. Brain. 2001; 124(Pt 4):739-56. DOI: 10.1093/brain/124.4.739. View

16.

Meador K, Loring D, Adams R, Patel B, Davis H, Hammond E . Central cholinergic systems and the P3 evoked potential. Int J Neurosci. 1987; 33(3-4):199-205. DOI: 10.3109/00207458708987404. View

17.

Sperling R, Greve D, Dale A, Killiany R, Holmes J, Rosas H . Functional MRI detection of pharmacologically induced memory impairment. Proc Natl Acad Sci U S A. 2002; 99(1):455-60. PMC: 117581. DOI: 10.1073/pnas.012467899. View

18.

Gevins A, Doyle J, Cutillo B, Schaffer R, Tannehill R, Ghannam J . Electrical potentials in human brain during cognition: new method reveals dynamic patterns of correlation. Science. 1981; 213(4510):918-22. DOI: 10.1126/science.7256287. View

19.

Gevins A, Cutillo B . Spatiotemporal dynamics of component processes in human working memory. Electroencephalogr Clin Neurophysiol. 1993; 87(3):128-43. DOI: 10.1016/0013-4694(93)90119-g. View

20.

Reches A, Laufer I, Ziv K, Cukierman G, McEvoy K, Ettinger M . Network dynamics predict improvement in working memory performance following donepezil administration in healthy young adults. Neuroimage. 2013; 88:228-41. PMC: 4096443. DOI: 10.1016/j.neuroimage.2013.11.020. View