Event-related delta and theta brain oscillations reflect age-related changes in both a general and a specific neuronal inhibitory mechanism

OBJECTIVE ERPs may be limited in validity when investigating inhibitory functions in later adulthood, as age-related increases in intraindividual variability and changes in EEG-oscillations are not considered. The present study compared averaged ERP peak and single trial time-frequency (TF) data analysis. METHODS Go/NoGo ERP waves amplitude/latency measures were compared with a TF analysis estimating single trial event-related EEG spectral power enhancement and intertrial phase-locking (ITC) in delta and theta band. RESULTS Age-related larger ITC was found for theta oscillations in the N2-P3 time range during NoGo, only. Discrepancies between N1/N2 ERP and TF results were obtained. Go/NoGo-P3 amplitude reductions in elderly were not related to an increased delta latency jitter. CONCLUSIONS Discrepancies between ERPs and TF results challenge conclusions made about age-related changes in Go/NoGo-N2. Earlier reports of age-related changes in P3 are supported by the present results. The study implies age-related impairments in a general neuronal inhibition mechanism and a specific response inhibition mechanism. SIGNIFICANCE The study indicates long-range communication impairments in the aged brain and the results are discussed considering hypotheses on increases in neural noise.

[1]  T W Picton,et al.  The effects of age on human event-related potentials. , 1984, Psychophysiology.

[2]  D. Mathalon,et al.  Event-related EEG time-frequency analysis: an overview of measures and an analysis of early gamma band phase locking in schizophrenia. , 2008, Schizophrenia bulletin.

[3]  K Richard Ridderinkhof,et al.  ERP components associated with successful and unsuccessful stopping in a stop-signal task. , 2004, Psychophysiology.

[4]  A. Starr,et al.  Effects of age on the P300 component of the event-related potential from auditory stimuli: peak definition, variation, and measurement. , 1985, Journal of gerontology.

[5]  Michael Falkenstein,et al.  Response inhibition subprocesses and dopaminergic pathways: Basal ganglia disease effects , 2010, Neuropsychologia.

[6]  J. Polich.  Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[7]  Ahmet Ademoglu,et al.  Wavelet Analysis of P3a and P3b , 2004, Brain Topography.

[8]  C. Basar-Eroglu,et al.  Event-related theta oscillations during working memory tasks in patients with schizophrenia and healthy controls. , 2005, Brain research. Cognitive brain research.

[9]  S. Luck.  An Introduction to the Event-Related Potential Technique , 2005 .

[10]  Sverker Sikström,et al.  Integrative neurocomputational perspectives on cognitive aging, neuromodulation, and representation , 2002, Neuroscience & Biobehavioral Reviews.

[11]  Erol Başar,et al.  Memory and Brain Dynamics: Oscillations Integrating Attention, Perception, Learning, and Memory , 2004 .

[12]  M. Fabiani,et al.  Individual differences in P3 scalp distribution in older adults, and their relationship to frontal lobe function. , 1998, Psychophysiology.

[13]  Laura Busse,et al.  Electrophysiological activity underlying inhibitory control processes in normal adults , 2006, Neuropsychologia.

[14]  Ziv M. Williams,et al.  From symphony to cacophony: Pathophysiology of the human basal ganglia in Parkinson disease , 2008, Neuroscience & Biobehavioral Reviews.

[15]  Kristine B Walhovd,et al.  P300 amplitude age reductions are not caused by latency jitter. , 2008, Psychophysiology.

[16]  Jonathan D. Cohen,et al.  Stimulus modality, perceptual overlap, and the go/no-go N2. , 2004, Psychophysiology.

[17]  Juliana Yordanova,et al.  Aging and error processing: Time-frequency analysis of error-related potentials. , 2005 .

[18]  M. Falkenstein.  Inhibition, conflict and the Nogo-N2 , 2006, Clinical Neurophysiology.

[19]  K. Walhovd,et al.  On the Topography of P3a and P3b Across the Adult Lifespan—A Factor-Analytic Study Using Orthogonal Procrustes Rotation , 2004, Brain Topography.

[20]  M. Falkenstein,et al.  Feedback-related processes during a time-production task in young and older adults , 2009, Clinical Neurophysiology.

[21]  S. MacDonald,et al.  Inconsistency in serial choice decision and motor reaction times dissociate in younger and older adults , 2004, Brain and Cognition.

[22]  M. Herrmann,et al.  Parkinson's disease and age-related alterations in brain oscillations during a Simon task , 2007, Neuroreport.

[23]  Juliana Yordanova,et al.  On the relation of movement-related potentials to the go/no-go effect on P3 , 2006, Biological Psychology.

[24]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

[25]  S. Sikström,et al.  Aging cognition: from neuromodulation to representation , 2001, Trends in Cognitive Sciences.

[26]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[27]  Anders M. Fjell,et al.  Instability in the latency of P3a/P3b brain potentials and cognitive function in aging , 2009, Neurobiology of Aging.

[28]  G. V. Simpson,et al.  ERP amplitude and scalp distribution to target and novel events: effects of temporal order in young, middle-aged and older adults. , 1994, Brain research. Cognitive brain research.

[29]  J. Hohnsbein,et al.  ERP components in Go/Nogo tasks and their relation to inhibition. , 1999, Acta psychologica.

[30]  R. Bakay,et al.  Aging-related changes in the nigrostriatal dopamine system and the response to MPTP in nonhuman primates: Diminished compensatory mechanisms as a prelude to parkinsonism , 2007, Neurobiology of Disease.

[31]  Tim Curran,et al.  EEG oscillations and recognition memory: Theta correlates of memory retrieval and decision making , 2006, NeuroImage.

[32]  T. Demiralp,et al.  P3 and delta band responses in visual oddball paradigm in schizophrenia , 2008, Neuroscience Letters.

[33]  D. Pizzagalli,et al.  When ‘go’ and ‘nogo’ are equally frequent: ERP components and cortical tomography , 2004, The European journal of neuroscience.

[34]  T. Salthouse,et al.  Methodological and theoretical implications of intraindividual variability in perceptual-motor performance. , 2004, The journals of gerontology. Series B, Psychological sciences and social sciences.

[35]  R. McCarley,et al.  The NoGo P300 ‘anteriorization’ effect and response inhibition , 2004, Clinical Neurophysiology.

[36]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[37]  Kaarin J. Anstey,et al.  Sensorimotor Variables and Forced Expiratory Volume as Correlates of Speed, Accuracy, and Variability in Reaction Time Performance in Late Adulthood , 1999 .

[38]  T. Demiralp,et al.  Comparative analysis of event-related potentials during Go/NoGo and CPT: Decomposition of electrophysiological markers of response inhibition and sustained attention , 2006, Brain Research.

[39]  D Friedman,et al.  An overview of age-related changes in the scalp distribution of P3b. , 1997, Electroencephalography and clinical neurophysiology.

[40]  Manuel Schabus,et al.  Fronto-parietal EEG coherence in theta and upper alpha reflect central executive functions of working memory. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[41]  T. Demiralp,et al.  Event-related theta oscillations: an integrative and comparative approach in the human and animal brain. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[42]  E. Strauss,et al.  Inconsistency in reaction time across the life span. , 2005, Neuropsychology.

[43]  Juliana Yordanova,et al.  Parallel systems of error processing in the brain , 2004, NeuroImage.

[44]  J. Ford,et al.  Age-related changes in auditory event-related potentials. , 1980, Electroencephalography and clinical neurophysiology.

[45]  F. Craik,et al.  Lapses of Intention and Performance Variability Reveal Age-Related Increases in Fluctuations of Executive Control , 2002, Brain and Cognition.

[46]  T. Shallice,et al.  Effects of focal frontal lesions on response inhibition. , 2006, Cerebral cortex.

[47]  J. Ford,et al.  ERPs to response production and inhibition. , 1985, Electroencephalography and clinical neurophysiology.

[48]  E Başar,et al.  A new approach to endogenous event-related potentials in man: relation between EEG and P300-wave. , 1984, The International journal of neuroscience.

[49]  J. Polich,et al.  Neuropsychology and neuropharmacology of P3a and P3b. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[50]  S. MacDonald,et al.  Neural underpinnings of within-person variability in cognitive functioning. , 2009, Psychology and aging.

[51]  A Kok,et al.  Varieties of inhibition: manifestations in cognition, event-related potentials and aging. , 1999, Acta psychologica.

[52]  T. Salthouse,et al.  Short-term variability in cognitive performance and the calibration of longitudinal change. , 2006, The journals of gerontology. Series B, Psychological sciences and social sciences.

[53]  R. Emmerson,et al.  Life-span changes in EEG spectral amplitude, amplitude variability and mean frequency , 1999, Clinical Neurophysiology.

[54]  J. Yordanova,et al.  Event-Related Oscillations and Cognitive Processes in Children A Review of Methodical Aspects and Empirical Findings , 2009 .

[55]  C. Basar-Eroglu,et al.  Altered oscillatory alpha and theta networks in schizophrenia , 2008, Brain Research.

[56]  W Schultz,et al.  Deficits in reaction times and movement times as correlates of hypokinesia in monkeys with MPTP-induced striatal dopamine depletion. , 1989, Journal of neurophysiology.

[57]  S. MacDonald,et al.  Intraindividual Variability in Vigilance Performance: Does Degrading Visual Stimuli Mimic Age-Related “Neural Noise”? , 2006, Journal of clinical and experimental neuropsychology.

[58]  Shane M. O’Mara,et al.  Individual differences discriminate event-related potentials but not performance during response inhibition , 2004, Experimental Brain Research.

[59]  E. Basar.  A study of the time and frequency characteristics of the potentials evoked in the acoustical cortex , 1972, Kybernetik.

[60]  K. R. Ridderinkhof,et al.  Electrophysiological correlates of anterior cingulate function in a go/no-go task: Effects of response conflict and trial type frequency , 2003, Cognitive, affective & behavioral neuroscience.

[61]  E. Jodo,et al.  Relation of a negative ERP component to response inhibition in a Go/No-go task. , 1992, Electroencephalography and clinical neurophysiology.

[62]  Michael Falkenstein,et al.  Inhibition-Related ERP Components: Variation with Modality, Age, and Time-on-Task , 2002 .

[63]  S. MacDonald,et al.  Simulating Neurocognitive Aging: Effects of a Dopaminergic Antagonist on Brain Activity During Working Memory , 2010, Biological Psychiatry.

[64]  E Pellouchoud,et al.  Neurophysiological signals of working memory in normal aging. , 2001, Brain research. Cognitive brain research.

[65]  J. Polich,et al.  EEG and ERP assessment of normal aging. , 1997, Electroencephalography and clinical neurophysiology.

[66]  Event-related potentials as indicators of repetition priming in young and older adults: amplitude, duration, and scalp distribution. , 1993, Psychology and aging.

[67]  Geert J. M. van Boxtel,et al.  The N2 in go/no-go tasks reflects conflict monitoring not response inhibition , 2004, Brain and Cognition.

[68]  E. Basar.  The theory of the whole-brain-work. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[69]  N. Squires,et al.  Electrophysiological correlates of categorization: P300 amplitude as index of target similarity , 2006, Biological Psychology.

[70]  C. N. Boehler,et al.  Sensory MEG responses predict successful and failed inhibition in a stop-signal task. , 2009, Cerebral cortex.

[71]  Georg Juckel,et al.  Dipole Localization of P300 and Normal Aging , 2004, Brain Topography.

[72]  S A Hillyard,et al.  Effects of aging on event-related brain potentials (ERPs) in a visual detection task. , 1994, Electroencephalography and clinical neurophysiology.

[73]  J. Rothwell,et al.  Cortical potentials related to the nogo decision , 2000, Experimental Brain Research.

[74]  H. Bokura,et al.  Electrophysiological correlates for response inhibition in a Go/NoGo task , 2001, Clinical Neurophysiology.

[75]  E. Basar,et al.  P300-response: possible psychophysiological correlates in delta and theta frequency channels. A review. , 1992, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[76]  E. Basar,et al.  Event-related oscillations are 'real brain responses'--wavelet analysis and new strategies. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[77]  J. Yordanova,et al.  Developmental changes in the event-related EEG theta response and P300. , 1997, Electroencephalography and clinical neurophysiology.

[78]  J. Hohnsbein,et al.  Late ERP components in visual and auditory Go/Nogo tasks. , 1995, Electroencephalography and clinical neurophysiology.

[79]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[80]  E. Basar,et al.  Gamma, alpha, delta, and theta oscillations govern cognitive processes. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[81]  Rita Y. Emmerson,et al.  Life Span Changes in Electrophysiological Measures of Inhibition , 1996, Brain and Cognition.

[82]  A Ademoglu,et al.  Decomposition of Event-Related Brain Potentials into Multiple Functional Components Using Wavelet Transform , 2001, Clinical EEG.

[83]  D. Tucker,et al.  Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation , 2004, Clinical Neurophysiology.

[84]  E. Basar,et al.  Please Scroll down for Article International Journal of Neuroscience Eeg, Auditory Evoked Potentials and Evoked Rhythmicities in Three-year-old Children , 2022 .

[85]  J. Kimura,et al.  Effects of aging on P3 components of somatosensory event-related potentials elicited by different stimulus conditions. Conventional averages and single-trial analysis. , 1996, The International journal of neuroscience.

[86]  A. Brand,et al.  Are oscillatory brain responses generally reduced in schizophrenia during long sustained attentional processing? , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[87]  C. Herrmann,et al.  Gamma responses and ERPs in a visual classification task , 1999, Clinical Neurophysiology.

[88]  L. Nyberg,et al.  Linking cognitive aging to alterations in dopamine neurotransmitter functioning: Recent data and future avenues , 2010, Neuroscience & Biobehavioral Reviews.

[89]  J. Polich,et al.  On the relationship between EEG and P300: individual differences, aging, and ultradian rhythms. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[90]  P. Holcomb,et al.  The effects of aging on the P3 component of the visual event-related potential. , 1985, Electroencephalography and clinical neurophysiology.

[91]  H. Semlitsch,et al.  Multichannel auditory event-related brain potentials: effects of normal aging on the scalp distribution of N1, P2, N2 and P300 latencies and amplitudes. , 1996, Electroencephalography and clinical neurophysiology.

[92]  G. Logan,et al.  In search of the point of no return: the control of response processes. , 1990, Journal of experimental psychology. Human perception and performance.

[93]  Manuel Schabus,et al.  Phase-locked alpha and theta oscillations generate the P1-N1 complex and are related to memory performance. , 2004, Brain research. Cognitive brain research.

[94]  D. Tucker,et al.  Regulating action: alternating activation of midline frontal and motor cortical networks , 2001, Clinical Neurophysiology.

[95]  Martin Eimer,et al.  Effects of attention and stimulus probability on ERPs in a Go/Nogo task , 1993, Biological Psychology.

[96]  A. Fallgatter,et al.  Age-related changes in the brain electrical correlates of response control , 1999, Clinical Neurophysiology.

[97]  Manuel Schabus,et al.  Theta coupling in the human electroencephalogram during a working memory task , 2004, Neuroscience Letters.

[98]  M Schürmann,et al.  The selectively distributed theta system: functions. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.