Effects of normal aging on event-related potentials and oscillatory brain activity during a haptic repetition priming task

This study reports neural repetition effects in young and older adults while performing a haptic repetition priming task consisting in the detection of the bilateral symmetry of familiar objects. To examine changes in event-related potentials (ERPs) and induced brain oscillations of object repetition priming with aging, we recorded EEGs of healthy groups of young (n=14; mean age=29.93 years) and older adults (n=15; mean age=66.4). Both groups exhibited similar behavioral haptic priming across repetitions, although young adults responded faster than the older group. Young and older adults showed ERP repetition enhancement at the 500-900 ms time window. In contrast, only the young participants showed ERP repetition suppression at the 1200-1500 ms segment. The results from the induced oscillations showed more positive amplitudes in young than in older adults at theta, alpha and beta frequencies (4-30 Hz). In addition, we found amplitude modulation related to stimulus repetition in the upper alpha and low beta sub-bands only in young adults (1250-1750 ms).The results suggest that although behavioral priming is spared with age, normal aging affects ERPs and oscillatory responses when performing an incidental priming symmetry detection task with haptically explored objects.

[1]  S. Geisser,et al.  On methods in the analysis of profile data , 1959 .

[2]  Soledad Ballesteros,et al.  Ageing affects brain activity in highly educated older adults: An ERP study using a word-stem priming task , 2010, Cortex.

[3]  D L Schacter,et al.  Implicit memory in amnesic patients: When is auditory priming spared? , 1995, Journal of the International Neuropsychological Society.

[4]  R. Klatzky,et al.  Haptic perception: A tutorial , 2009, Attention, perception & psychophysics.

[5]  David Friedman,et al.  Changes in familiarity and recollection across the lifespan: An ERP perspective , 2010, Brain Research.

[6]  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.

[7]  Soledad Ballesteros,et al.  Visual and Haptic Discrimination of Symmetry in Unfamiliar Displays Extended in the z-Axis , 2004, Perception.

[8]  S Millar,et al.  Symmetry in haptic and in visual shape perception , 1998, Perception & psychophysics.

[9]  Auditory priming: implicit and explicit memory for words and voices. , 1992 .

[10]  L L Light,et al.  Adult age differences in repetition priming: a meta-analysis. , 1994, Psychology and aging.

[11]  M Doppelmayr,et al.  A method for the calculation of induced band power: implications for the significance of brain oscillations. , 1998, Electroencephalography and clinical neurophysiology.

[12]  W. De Clercq,et al.  Automatic Removal of Ocular Artifacts in the EEG without an EOG Reference Channel , 2006, Proceedings of the 7th Nordic Signal Processing Symposium - NORSIG 2006.

[13]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[14]  S. Ballesteros,et al.  Haptic discrimination of bilateral symmetry in 2-dimensional and 3-dimensional unfamiliar displays , 1997, Perception & psychophysics.

[15]  Soledad Ballesteros,et al.  Implicit and explicit memory for familiar and novel objects presented to touch , 1999 .

[16]  W. Klimesch,et al.  What does phase information of oscillatory brain activity tell us about cognitive processes? , 2008, Neuroscience & Biobehavioral Reviews.

[17]  S. Rossi,et al.  Human cortical responses during one-bit short-term memory. A high-resolution EEG study on delayed choice reaction time tasks , 2004, Clinical Neurophysiology.

[18]  R. Klatzky,et al.  Hand movements: A window into haptic object recognition , 1987, Cognitive Psychology.

[19]  Matthias M. Müller,et al.  Oscillatory brain activity dissociates between associative stimulus content in a repetition priming task in the human EEG. , 2004, Cerebral cortex.

[20]  M. Laine,et al.  Effects of normal aging on event-related desynchronization/synchronization during a memory task in humans , 2004, Neuroscience Letters.

[21]  Michael C. Doyle,et al.  Modulation of event-related potentials by the repetition of drawings of novel objects. , 1995, Brain research. Cognitive brain research.

[22]  F. Craik,et al.  Age differences in recall and recognition , 1987 .

[23]  C. Joyce,et al.  Memory changes with normal aging: behavioral and electrophysiological measures. , 1998, Psychophysiology.

[24]  S. Ballesteros,et al.  Implicit and Explicit Memory for Visual and Haptic Objects: Cross-Modal Priming Depends on Structural Descriptions , 1999 .

[25]  R L Klatzky,et al.  Identifying objects by touch: An “expert system” , 1985, Perception & psychophysics.

[26]  Yang Jiang,et al.  Age effects on brain activity during repetition priming of targets and distracters , 2007, Neuropsychologia.

[27]  Martin Grunwald,et al.  Power of theta waves in the EEG of human subjects increases during recall of haptic information , 1999, Neuroscience Letters.

[28]  F. Kruggel,et al.  Theta-power Differences in Patients with Mild Cognitive Impairment Under Rest Condition and During Haptic Tasks , 2002, Alzheimer disease and associated disorders.

[29]  Yang Liu,et al.  Diurnal variations in alpha power density and subjective sleepiness while performing repeated vigilance tasks , 2001, Clinical Neurophysiology.

[30]  E Tulving,et al.  Priming and human memory systems. , 1990, Science.

[31]  Debra A. Fleischman,et al.  Repetition Priming in Aging and Alzheimer's Disease: An Integrative Review and Future Directions , 2007, Cortex.

[32]  Hideko F. Norman,et al.  Aging and the Visual, Haptic, and Cross-Modal Perception of Natural Object Shape , 2006, Perception.

[33]  Alex Martin,et al.  Repetition Priming Across the Adult Lifespan—The Long and Short of It , 2006, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[34]  T. Sejnowski,et al.  Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects , 2000, Clinical Neurophysiology.

[35]  W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[36]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

[37]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[38]  D. Friedman,et al.  Repetition priming of possible and impossible objects from ERP and behavioral perspectives. , 2006, Psychophysiology.

[39]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

[40]  Peter J. Gianaros,et al.  Handbook of Psychophysiology: Methodology , 2007 .

[41]  J G Snodgrass,et al.  ERPs during study as a function of subsequent direct and indirect memory testing in young and old adults. , 1996, Brain research. Cognitive brain research.

[42]  J. Grainger,et al.  Exploring the temporal dynamics of visual word recognition in the masked repetition priming paradigm using event-related potentials , 2007, Brain Research.

[43]  Axel Mecklinger,et al.  Priming and recognition of novel 3D objects: Guidance from event-related potentials , 2000 .

[44]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.

[45]  S. Rossi,et al.  Human cortical rhythms during visual delayed choice reaction time tasks A high-resolution EEG study on normal aging , 2004, Behavioural Brain Research.

[46]  Soledad Ballesteros,et al.  Ageing affects event-related potentials and brain oscillations: A behavioral and electrophysiological study using a haptic recognition memory task , 2011, Neuropsychologia.

[47]  W. Klimesch,et al.  Theta synchronization during episodic retrieval: neural correlates of conscious awareness. , 2001, Brain research. Cognitive brain research.

[48]  Christian Gerloff,et al.  Larger interregional synchrony is associated with greater behavioral success in a complex sensory integration task in humans. , 2005, Cerebral cortex.

[49]  R. Roberts,et al.  Word repetition effects on event-related potentials in healthy young and old subjects, and in patients with alzheimer-type dementia , 1994, Neuropsychologia.

[50]  C. C. Wood,et al.  Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. , 1985, Electroencephalography and clinical neurophysiology.

[51]  Rebecca Lawson,et al.  Repetition priming and the haptic recognition of familiar and unfamiliar objects , 2008, Perception & psychophysics.

[52]  M. Bryden Measuring handedness with questionnaires , 1977, Neuropsychologia.

[53]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[54]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[55]  N. Raz,et al.  Differential effects of aging on memory for content and context: a meta-analysis. , 1995, Psychology and aging.

[56]  S. Ballesteros,et al.  Intact haptic priming in normal aging and Alzheimer’s disease: evidence for dissociable memory systems , 2004, Neuropsychologia.

[57]  C S Herrmann,et al.  Magnetoencephalographic responses to illusory figures: early evoked gamma is affected by processing of stimulus features. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[58]  W. Klimesch,et al.  Induced alpha band power changes in the human EEG and attention , 1998, Neuroscience Letters.

[59]  M. Heller,et al.  Selective attention modulates visual and haptic repetition priming: effects in aging and Alzheimer's disease , 2008, Experimental Brain Research.

[60]  Marc W Howard,et al.  Theta and Gamma Oscillations during Encoding Predict Subsequent Recall , 2003, The Journal of Neuroscience.

[61]  R. Oostenveld,et al.  Theta and Gamma Oscillations Predict Encoding and Retrieval of Declarative Memory , 2006, The Journal of Neuroscience.

[62]  S. Bressler,et al.  Response preparation and inhibition: The role of the cortical sensorimotor beta rhythm , 2008, Neuroscience.

[63]  D A Fleischman,et al.  Repetition priming in normal aging and Alzheimer's disease: a review of findings and theories. , 1998, Psychology and aging.

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

[65]  S Makeig,et al.  Blind separation of auditory event-related brain responses into independent components. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[67]  S. Makeig,et al.  Section: Behavioral/systems/cognitive Medial Prefrontal Theta Bursts Precede Rapid Motor Responses during Visual Selective Attention Introduction , 2022 .

[68]  J. M. D. L. Iglesia,et al.  Versión española del cuestionario de Yesavage abreviado (GDS) para el despistaje de depresión en mayores de 65 años: adaptación y validación , 2002 .

[69]  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.

[70]  E. Bushnell,et al.  Children's haptic and cross-modal recognition with familiar and unfamiliar objects. , 1999, Journal of Experimental Psychology: Human Perception and Performance.

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

[72]  V. Leirer,et al.  Development and validation of a geriatric depression screening scale: a preliminary report. , 1982, Journal of psychiatric research.

[73]  D. B. Mitchell,et al.  Age differences in implicit memory: conceptual, perceptual, or methodological? , 2003, Psychology and aging.

[74]  Lars Kai Hansen,et al.  ERPWAVELAB A toolbox for multi-channel analysis of time–frequency transformed event related potentials , 2007, Journal of Neuroscience Methods.

[75]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[76]  A. Leuthold,et al.  Beta-Band Activity during Motor Planning Reflects Response Uncertainty , 2010, The Journal of Neuroscience.

[77]  A. E. Schulman,et al.  Functional coupling of human cortical sensorimotor areas during bimanual skill acquisition. , 1999, Brain : a journal of neurology.

[78]  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.

[79]  H. Lüders,et al.  American Electroencephalographic Society Guidelines for Standard Electrode Position Nomenclature , 1991, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[80]  Daniel L. Schacter,et al.  Priming and recognition of transformed three-dimensional objects: effects of size and reflection. , 1992 .

[81]  Simon Finnigan,et al.  Theta power is reduced in healthy cognitive aging. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[82]  E. Carmeli,et al.  The aging hand. , 2003, The journals of gerontology. Series A, Biological sciences and medical sciences.

[83]  Arnaud Delorme,et al.  Frontal midline EEG dynamics during working memory , 2005, NeuroImage.

[84]  Craig J. Brozinsky,et al.  Oscillatory EEG correlates of episodic trace decay. , 2006, Cerebral cortex.

[85]  Marianna D. Eddy,et al.  Electrophysiological evidence for size invariance in masked picture repetition priming , 2009, Brain and Cognition.

[86]  Michael D. Rugg,et al.  Dissociation of the neural correlates of implicit and explicit memory , 1998, Nature.

[87]  W Krause,et al.  Theta power in the EEG of humans during ongoing processing in a haptic object recognition task. , 2001, Brain research. Cognitive brain research.

[88]  T. Penney,et al.  Repetition related ERP effects in a visual object target detection task. , 2001, Brain research. Cognitive brain research.

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

[90]  Soledad Ballesteros,et al.  The effect of age on word-stem cued recall: A behavioral and electrophysiological study , 2009, Brain Research.

[91]  Axel Mecklinger,et al.  Feature binding in perceptual priming and in episodic object recognition: evidence from event-related brain potentials. , 2005, Brain research. Cognitive brain research.

[92]  Denise C. Park,et al.  Please Scroll down for Article European Journal of Cognitive Psychology Effects of Ageing on Associative Memory for Related and Unrelated Pictures , 2022 .

[93]  Bernhard Pastötter,et al.  Oscillatory correlates of controlled speed‐accuracy tradeoff in a response‐conflict task , 2012, Human brain mapping.