Age-associated modulations of cerebral oscillatory patterns related to attention control

Visual attention depends on bottom-up sensory activation and top-down attentional guidance. Although aging is known to affect sensory processing, its impact on the top-down control of attention remains a matter of debate. We investigated age-related modulations of brain oscillatory activity during visual attention using a variant of the attention network test (ANT) in 20 young and 28 elderly adults. We examined the EEG oscillatory responses to warning and target signals, and explored the correlates of temporal and spatial orienting as well as conflict resolution at target presentation. Time-frequency analysis was performed between 4 and 30 Hz, and the relationship between behavioral and brain oscillatory responses was analyzed. Whereas temporal cueing and conflict had similar reaction time effects in both age groups, spatial cueing was more beneficial to older than younger subjects. In the absence of cue, posterior alpha activation was drastically reduced in older adults, pointing to an age-related decline in anticipatory attention. Following both cues and targets, older adults displayed pronounced motor-related activation in the low beta frequency range at the expense of attention-related posterior alpha activation prominent in younger adults. These findings support the recruitment of alternative motor-related circuits in the elderly, in line with the dedifferentiation hypothesis. Furthermore, older adults showed reduced midparietal alpha inhibition induced by temporal orienting as well as decreased posterior alpha activation associated with both spatial orienting and conflict resolution. Altogether, the results are consistent with an overall reduction of task-related alpha activity in the elderly, and provide functional evidence that younger and older adults engage distinct brain circuits at different oscillatory frequencies during attentional functions.

[1]  Panteleimon Giannakopoulos,et al.  Face short-term memory-related electroencephalographic patterns can differentiate multi- versus single-domain amnestic mild cognitive impairment. , 2011, Journal of Alzheimer's disease : JAD.

[2]  Jin Fan,et al.  The activation of attentional networks , 2005, NeuroImage.

[3]  Aneta Brzezicka,et al.  β band oscillations as a correlate of alertness--changes in aging. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[4]  M. Carrasco Covert attention increases contrast sensitivity: Psychophysical, neurophysiological and neuroimaging studies. , 2006, Progress in brain research.

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

[6]  Jose-Manuel Alonso,et al.  Fundamentals of vision : low and mid-level processes in perception , 2006 .

[7]  L. Capranica,et al.  Effects of Aging on Visual Attentional Focusing , 2005, Gerontology.

[8]  Wolfgang Klimesch,et al.  Alpha Oscillations and Early Stages of Visual Encoding , 2011, Front. Psychology.

[9]  John J. Foxe,et al.  The Role of Alpha-Band Brain Oscillations as a Sensory Suppression Mechanism during Selective Attention , 2011, Front. Psychology.

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

[11]  G. Thut,et al.  Mechanisms of selective inhibition in visual spatial attention are indexed by α‐band EEG synchronization , 2007, The European journal of neuroscience.

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

[13]  N. Birbaumer,et al.  Event-related beta desynchronization indicates timing of response selection in a delayed-response paradigm in humans , 2001, Neuroscience Letters.

[14]  N. Ward Compensatory mechanisms in the aging motor system , 2006, Ageing Research Reviews.

[15]  Richard S. Frackowiak,et al.  Aging is associated with contrasting changes in local and distant cortical connectivity in the human motor system , 2006, NeuroImage.

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

[17]  David Lester Neumann,et al.  The Effect of Associative and Dissociative Attentional Focus Strategies on Muscle Activity and Heart Rate During a Weight Training Exercise , 2011 .

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

[19]  G. Curio,et al.  Task‐related differential dynamics of EEG alpha‐ and beta‐band synchronization in cortico‐basal motor structures , 2007, The European journal of neuroscience.

[20]  T. Salthouse The processing-speed theory of adult age differences in cognition. , 1996, Psychological review.

[21]  Catherine Tallon-Baudry,et al.  Induced γ-Band Activity during the Delay of a Visual Short-Term Memory Task in Humans , 1998, The Journal of Neuroscience.

[22]  C. Cavallero,et al.  Age-Related Differences in the Attention Network Test (ANT) , 2010, Experimental aging research.

[23]  G. Pfurtscheller Central beta rhythm during sensorimotor activities in man. , 1981, Electroencephalography and clinical neurophysiology.

[24]  C. Gerloff,et al.  The influence of normal aging on the cortical processing of a simple motor task , 2000, Neurology.

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

[26]  V. Ibáñez,et al.  EEG alpha activity reflects motor preparation rather than the mode of action selection , 2012, Front. Integr. Neurosci..

[27]  Eric Hahn,et al.  Event-related potentials associated with Attention Network Test. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[28]  G. Pfurtscheller,et al.  Functional brain imaging based on ERD/ERS , 2001, Vision Research.

[29]  B. Schneider,et al.  Implications of perceptual deterioration for cognitive aging research. , 2000 .

[30]  J. Pernier,et al.  Induced gamma-band activity during the delay of a visual short-term memory task in humans. , 1998, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Gert Pfurtscheller,et al.  Desynchronization and recovery of β rhythms during brisk and slow self-paced finger movements in man , 1995, Neuroscience Letters.

[32]  P. Whalen Fear, Vigilance, and Ambiguity , 1998 .

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

[34]  R. West,et al.  An application of prefrontal cortex function theory to cognitive aging. , 1996, Psychological bulletin.

[35]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[36]  Manuel Schabus,et al.  A shift of visual spatial attention is selectively associated with human EEG alpha activity , 2005, The European journal of neuroscience.

[37]  Yaakov Stern,et al.  The effects of aging on time reproduction in delayed free-recall , 2005, Brain and Cognition.

[38]  Jin Fan,et al.  Age-related differences in attentional networks of alerting and executive control in young, middle-aged, and older Chinese adults , 2011, Brain and Cognition.

[39]  J. Richiardi,et al.  Attention-Related Potentials Allow for a Highly Accurate Discrimination of Mild Cognitive Impairment Subtypes , 2012, Neurodegenerative Diseases.

[40]  V. Ibáñez,et al.  Aging effects on selective attention-related electroencephalographic patterns during face encoding , 2010, Neuroscience.

[41]  P. Baltes,et al.  Emergence of a powerful connection between sensory and cognitive functions across the adult life span: a new window to the study of cognitive aging? , 1997, Psychology and aging.

[42]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[43]  P A Hancock,et al.  The effects of sex, age, and interval duration on the perception of time. , 2010, Acta psychologica.

[44]  P. Derambure,et al.  Oscillatory cortical activity related to voluntary muscle relaxation: Influence of normal aging , 2006, Clinical Neurophysiology.

[45]  Adam Gazzaley,et al.  Age-Related Changes in Orienting Attention in Time , 2011, The Journal of Neuroscience.

[46]  George V. Rebec,et al.  A new perspective on behavioral inconsistency and neural noise in aging: compensatory speeding of neural communication , 2012, Frontiers in aging neuroscience.

[47]  Avishai Henik,et al.  Temporal Orienting and Alerting – The Same or Different? , 2012, Front. Psychology.

[48]  Claude-Alain Hauert,et al.  Programming effectors and coordination in bimanual in-phase mirror finger movements. , 2005, Brain research. Cognitive brain research.

[49]  Dale Dagenbach,et al.  Age-Related Changes and the Attention Network Task: An Examination of Alerting, Orienting, and Executive Function , 2007, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[50]  Antonino Vallesi,et al.  Age effects on the asymmetry of the motor system: Evidence from cortical oscillatory activity , 2010, Biological Psychology.

[51]  David J. Madden,et al.  Aging and Visual Attention , 2007, Current directions in psychological science.

[52]  Bruce D. McCandliss,et al.  Testing the Efficiency and Independence of Attentional Networks , 2002, Journal of Cognitive Neuroscience.

[53]  Monica Fabiani,et al.  Reduced Suppression or Labile Memory? Mechanisms of Inefficient Filtering of Irrelevant Information in Older Adults , 2006, Journal of Cognitive Neuroscience.

[54]  J. Birren,et al.  Aging and speed of behavior: possible consequences for psychological functioning. , 1995, Annual review of psychology.

[55]  Jeffrey W. Cooney,et al.  Top-down suppression deficit underlies working memory impairment in normal aging , 2005, Nature Neuroscience.

[56]  Diego Fernandez-Duque,et al.  Attentional networks in normal aging and Alzheimer's disease. , 2006, Neuropsychology.

[57]  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.

[58]  Hauke R. Heekeren,et al.  What Happens in Between? Human Oscillatory Brain Activity Related to Crossmodal Spatial Cueing , 2008, PloS one.

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

[60]  R. Desimone,et al.  Neural mechanisms of spatial selective attention in areas V1, V2, and V4 of macaque visual cortex. , 1997, Journal of neurophysiology.

[61]  Bruce D. McCandliss,et al.  Response Anticipation and Response Conflict: An Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2007, The Journal of Neuroscience.

[62]  C. Brunia,et al.  Anticipatory attention: an event-related desynchronization approach. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[64]  P. Derambure,et al.  Influence of aging on cortical activity associated with a visuo-motor task , 2004, Neurobiology of Aging.

[65]  D. Filion,et al.  Aging, selective attention, and inhibitory processes: a psychophysiological approach. , 1992, Psychology and Aging.

[66]  T. Curran,et al.  Effects of aging on visuospatial attention: an ERP study , 2001, Neuropsychologia.

[67]  I. THE ATTENTION SYSTEM OF THE HUMAN BRAIN , 2002 .

[68]  Edward J. Golob,et al.  Event-related potentials accompanying motor preparation and stimulus expectancy in the young, young-old and oldest-old , 2005, Neurobiology of Aging.

[69]  M. Fabiani It was the best of times, it was the worst of times: a psychophysiologist's view of cognitive aging. , 2012, Psychophysiology.

[70]  M. Kawato,et al.  Attentional shifts towards an expected visual target alter the level of alpha-band oscillatory activity in the human calcarine cortex. , 2005, Brain research. Cognitive brain research.

[71]  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.

[72]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[73]  E. Vogel,et al.  Sensory gain control (amplification) as a mechanism of selective attention: electrophysiological and neuroimaging evidence. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[74]  P. D. Spear,et al.  Neural bases of visual deficits during aging , 1993, Vision Research.

[75]  Lynn Hasher,et al.  Working Memory, Comprehension, and Aging: A Review and a New View , 1988 .

[76]  Michael Erb,et al.  Separation of phasic arousal and expectancy effects in a speeded reaction time task via fMRI. , 2009, Psychophysiology.

[77]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

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

[79]  G. Pfurtscheller,et al.  Event-related synchronization of mu rhythm in the EEG over the cortical hand area in man , 1994, Neuroscience Letters.

[80]  R. Desimone,et al.  Selective attention gates visual processing in the extrastriate cortex. , 1985, Science.

[81]  M. Westerfield,et al.  Modality-specificity of sensory aging in vision and audition: Evidence from event-related potentials , 2008, Brain Research.

[82]  Bruce D. McCandliss,et al.  The Relation of Brain Oscillations to Attentional Networks , 2007, The Journal of Neuroscience.

[83]  Raymond M. Klein,et al.  Repeated Measurement of the Components of Attention of Older Adults using the Two Versions of the Attention Network Test: Stability, Isolability, Robustness, and Reliability , 2011, Front. Ag. Neurosci..

[84]  A. Engel,et al.  Beta-band oscillations—signalling the status quo? , 2010, Current Opinion in Neurobiology.

[85]  Brian R Ott,et al.  Interactions between phasic alerting and spatial orienting: effects of normal aging and Alzheimer's disease. , 2004, Neuropsychology.

[86]  Sylvie Belleville,et al.  Age-related differences in response preparation: the role of time uncertainty. , 2004, The journals of gerontology. Series B, Psychological sciences and social sciences.

[87]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[88]  Todd S. Braver,et al.  Working Memory, Executive Control, and Aging , 2007 .

[89]  Wilfried Lang,et al.  Reduced activation of midline frontal areas in human elderly subjects: a contingent negative variation study , 2000, Neuroscience Letters.

[90]  P. Brown,et al.  Lateralization of event-related beta desynchronization in the EEG during pre-cued reaction time tasks , 2005, Clinical Neurophysiology.

[91]  O. Jensen,et al.  Shaping Functional Architecture by Oscillatory Alpha Activity: Gating by Inhibition , 2010, Front. Hum. Neurosci..

[92]  A. Nobre,et al.  Alpha Oscillations Related to Anticipatory Attention Follow Temporal Expectations , 2011, The Journal of Neuroscience.

[93]  Peter S. Jones,et al.  Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study , 2006, NeuroImage.