Combined frontal and parietal P300 amplitudes indicate compensated cognitive processing across the lifespan

In the present study the frontal and parietal P300, elicited in an auditory oddball paradigm were investigated in a large sample of healthy participants (N = 1572), aged 6–87. According to the concepts of the compensation-related utilization of neural circuits hypothesis (CRUNCH) it was hypothesized that the developmental trajectories of the frontal P300 would reach a maximum in amplitude at an older age than the amplitude of the parietal P300 amplitude. In addition, the amplitude of the frontal P300 was expected to increase with aging in adulthood in contrast to a decline in amplitude of the parietal P300 amplitude. Using curve-fitting methods, a comparison was made between the developmental trajectories of the amplitudes of the frontal and parietal P300. It was found that the developmental trajectories of frontal and parietal P300 amplitudes differed significantly across the lifespan. During adulthood, the amplitude of the parietal P300 declines with age, whereas both the frontal P300 amplitude and behavioral performance remain unaffected. A lifespan trajectory of combined frontal and parietal P300 amplitudes was found to closely resemble the lifespan trajectory of behavioral performance. Our results can be understood within the concepts of CRUNCH. That is, to compensate for declining neural resources, older participants recruit additional neural resources of prefrontal origin and consequently preserve a stable behavioral performance. Though, a direct relation between amplitude of the frontal P300 and compensatory mechanisms cannot yet be claimed.

[1]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[2]  H G Vaughan,et al.  Averaged Evoked Responses in Vigilance and Discrimination: A Reassessment , 1969, Science.

[3]  M. McCabe.  Presidential address. , 1970, Irish nurses' journal.

[4]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[5]  S. Hillyard,et al.  Long-latency evoked potentials to irrelevant, deviant stimuli. , 1976, Behavioral biology.

[6]  William L. Wilkie,et al.  Presidential Address: 1980 , 1981 .

[7]  B. Kopell,et al.  The Stroop effect: brain potentials localize the source of interference. , 1981, Science.

[8]  E. Donchin.  Presidential address, 1980. Surprise!...Surprise? , 1981, Psychophysiology.

[9]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[10]  M. Kutas,et al.  Electrophysiology of cognitive processing. , 1983, Annual review of psychology.

[11]  R Galambos,et al.  Autism: processing of novel auditory information assessed by event-related brain potentials. , 1984, Electroencephalography and clinical neurophysiology.

[12]  R. Thatcher,et al.  Human cerebral hemispheres develop at different rates and ages. , 1987, Science.

[13]  R. Verleger.  Event-related potentials and cognition: A critique of the context updating hypothesis and an alternative interpretation of P3 , 1988, Behavioral and Brain Sciences.

[14]  J. Polich,et al.  Meta-analysis of P300 normative aging studies. , 1996, Psychophysiology.

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

[16]  S. J. Steiner,et al.  A new method for off-line robot programming: applications and limitations using a virtual environment , 1997 .

[17]  J. Polich,et al.  P3a and P3b from typical auditory and visual stimuli , 1999, Clinical Neurophysiology.

[18]  K. Walhovd,et al.  Two- and three-stimuli auditory oddball ERP tasks and neuropsychological measures in aging , 2001, Neuroreport.

[19]  Roberto Cabeza,et al.  Aging Gracefully: Compensatory Brain Activity in High-Performing Older Adults , 2002, NeuroImage.

[20]  D. Friedman.  Cognition and Aging: A Highly Selective Overview of Event-Related Potential (ERP) Data , 2003, Journal of clinical and experimental neuropsychology.

[21]  D. Rujescu,et al.  The neural basis of the P300 potential. Focus on the time-course of the underlying cortical generators. , 2004, European archives of psychiatry and clinical neuroscience.

[22]  D. Rujescu,et al.  The neural basis of the P300 potential , 2004, European Archives of Psychiatry and Clinical Neuroscience.

[23]  J. Polich.  Clinical application of the P300 event-related brain potential. , 2004, Physical medicine and rehabilitation clinics of North America.

[24]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[25]  D. Linden.  The P300: Where in the Brain Is It Produced and What Does It Tell Us? , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[26]  Salil H. Patel,et al.  Characterization of N200 and P300: Selected Studies of the Event-Related Potential , 2005, International journal of medical sciences.

[27]  E. Gordon,et al.  THE TEST-RETEST RELIABILITY OF A STANDARDIZED NEUROCOGNITIVE AND NEUROPHYSIOLOGICAL TEST BATTERY: “NEUROMARKER” , 2005, The International journal of neuroscience.

[28]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[29]  Leanne M Williams,et al.  Standardized assessment of cognitive functioning during development and aging using an automated touchscreen battery. , 2006, Archives of clinical neuropsychology : the official journal of the National Academy of Neuropsychologists.

[30]  S. Makeig,et al.  Imaging human EEG dynamics using independent component analysis , 2006, Neuroscience & Biobehavioral Reviews.

[31]  E. Gordon,et al.  CROSS-CULTURAL ASSESSMENT OF NEUROPSYCHOLOGICAL PERFORMANCE AND ELECTRICAL BRAIN FUNCTION MEASURES: ADDITIONAL VALIDATION OF AN INTERNATIONAL BRAIN DATABASE , 2007, The International journal of neuroscience.

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

[33]  R. Cabeza,et al.  Que PASA? The posterior-anterior shift in aging. , 2008, Cerebral cortex.

[34]  P. Reuter-Lorenz,et al.  Neurocognitive Aging and the Compensation Hypothesis , 2008 .

[35]  Ki-Young Jung,et al.  Influence of task difficulty on the features of event-related potential during visual oddball task , 2008, Neuroscience Letters.

[36]  J. Polich.  Updating P 300 : An Integrative Theory of P 3 a and P 3 b , 2009 .

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

[38]  Ki-Young Jung,et al.  Changes in gamma- and theta-band phase synchronization patterns due to the difficulty of auditory oddball task , 2010, Neuroscience Letters.

[39]  Patricia A. Reuter-Lorenz,et al.  Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load , 2010, Cortex.

[40]  Hillary D. Schwarb,et al.  The influence of age and individual differences in executive function on stimulus processing in the oddball task , 2010, Cortex.

[41]  Phillip J. Holcomb,et al.  Mechanisms Underlying Age- and Performance-related Differences in Working Memory , 2011, Journal of Cognitive Neuroscience.

[42]  E. Paulesu,et al.  Reassessing the HAROLD model: Is the hemispheric asymmetry reduction in older adults a special case of compensatory-related utilisation of neural circuits? , 2013, Experimental Brain Research.

[43]  C. Grady.  The cognitive neuroscience of ageing , 2012, Nature Reviews Neuroscience.

[44]  R. O’Connell,et al.  A simultaneous ERP/fMRI investigation of the P300 aging effect , 2012, Neurobiology of Aging.

[45]  Natasha M. Maurits,et al.  Compensation through Increased Functional Connectivity: Neural Correlates of Inhibition in Old and Young , 2012, Journal of Cognitive Neuroscience.

[46]  S. Kelly,et al.  A supramodal accumulation-to-bound signal that determines perceptual decisions in humans , 2012, Nature Neuroscience.

[47]  R. Knight,et al.  Age-related frontoparietal changes during the control of bottom-up and top-down attention: an ERP study , 2013, Neurobiology of Aging.

[48]  S. Kelly,et al.  Internal and External Influences on the Rate of Sensory Evidence Accumulation in the Human Brain , 2013, The Journal of Neuroscience.

[49]  B. Gallhofer,et al.  The impact of age on load-related dorsolateral prefrontal cortex activation , 2014, Front. Aging Neurosci..

[50]  M. Arns,et al.  P300 Development across the Lifespan: A Systematic Review and Meta-Analysis , 2014, PloS one.

[51]  Rolf Verleger,et al.  Testing the stimulus-to-response bridging function of the oddball-P3 by delayed response signals and residue iteration decomposition (RIDE) , 2014, NeuroImage.

[52]  Less wiring, more firing: low-performing older adults compensate for impaired white matter integrity with increased neural activity , 2014 .

[53]  Vijeth Iyengar,et al.  Less wiring, more firing: low-performing older adults compensate for impaired white matter with greater neural activity. , 2015, Cerebral cortex.

[54]  W. Ziegler.  The Oxford Handbook Of Event Related Potential Components , 2016 .

[55]  Marina Schmid,et al.  An Introduction To The Event Related Potential Technique , 2016 .