Age-related deficits in efficiency of low-level lateral inhibition

Background: In a masked prime task using a 0 ms prime-target inter-stimulus-interval, responses on trials where prime and target match (compatible trials) are usually faster and more accurate than responses where prime and target mismatch (incompatible trials). This positive compatibility effect (PCE) comprises both behavioral benefits on compatible relative to neutral trials, and behavioral costs on incompatible relative to neutral trials. Comparing performance in 2- vs. 4-alternative-response versions of the task indicates that benefits are due to direct priming (i.e., pre-activation) of a motor response, whereas costs reflect an inhibition of the alternative response tendency. The present study employs this paradigm to test the hypothesis that normal aging is associated with a selective deficit in inhibitory function, affecting both low-level motor and higher-level executive control. Experiment and Results: Testing 20 young and 20 older healthy adults, we found that (1) overall, prime-induced benefits were of similar magnitude across age groups, but inhibition-based costs were smaller in older compared to young adults; (2) increasing the number of response alternatives caused the same pattern of unaltered benefits and reduced costs in both age groups; and (3) costs, but not benefits, in the 2-alternative condition were significantly predicted by scores on the digit symbol substitution task (DSST), independently of age and other background variables. Interpretation: Results demonstrate the possibility of isolating an inhibitory component in low-level perceptuo-motor control. Importantly, this component shows an age-related decline in the absence of a corresponding decline of visuo-motor excitability, and appears to be linked to performance on a higher-level processing speed task. We hypothesize that aging might affect the brain's ability to establish precise short-term lateral inhibitory links, and that even in young adults, the efficiency of such links is a significant contributing factor in higher-level cognitive performance.

[1]  Lynn Hasher,et al.  Distraction as a determinant of processing speed , 2006, Psychonomic bulletin & review.

[2]  M. Eimer,et al.  Locus of Inhibition in the Masked Priming of Response Alternatives , 2002, Journal of motor behavior.

[3]  Petroc Sumner,et al.  Tight coupling between positive and reversed priming in the masked prime paradigm. , 2010, Journal of experimental psychology. Human perception and performance.

[4]  T. Salthouse What and When of Cognitive Aging , 2004 .

[5]  Stuart T Klapp,et al.  Either or neither, but not both: locating the effects of masked primes , 2009, Proceedings of the Royal Society B: Biological Sciences.

[6]  Cynthia P. May,et al.  Inhibitory control, circadian arousal, and age. , 1999 .

[7]  K. Walhovd,et al.  Structural Brain Changes in Aging: Courses, Causes and Cognitive Consequences , 2010, Reviews in the neurosciences.

[8]  H. Bowman,et al.  Dissociating local and global levels of perceptuo-motor control in masked priming , 2006 .

[9]  W. E. Hick Quarterly Journal of Experimental Psychology , 1948, Nature.

[10]  K. R. Ridderinkhof,et al.  Error-related brain potentials are differentially related to awareness of response errors: evidence from an antisaccade task. , 2001, Psychophysiology.

[11]  B A Silverstein,et al.  Effects of age, sex, and anthropometric factors on nerve conduction measures , 1992, Muscle & nerve.

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

[13]  Christina Wasylyshyn,et al.  Adult age and digit symbol substitution performance: a meta-analysis. , 2004, Psychology and aging.

[14]  Annette Sterr,et al.  Neural correlates of movement preparation in healthy ageing , 2007, The European journal of neuroscience.

[15]  Johannes J. Fahrenfort,et al.  Pre-SMA Gray-matter Density Predicts Individual Differences in Action Selection in the Face of Conscious and Unconscious Response Conflict , 2011, Journal of Cognitive Neuroscience.

[16]  Christophe Tandonnet,et al.  Selective suppression of the incorrect response implementation in choice behavior assessed by transcranial magnetic stimulation. , 2011, Psychophysiology.

[17]  Franck Vidal,et al.  Neural inhibition and interhemispheric connections in two-choice reaction time: a Laplacian ERP study. , 2009, Psychophysiology.

[18]  C. Kennard,et al.  Human Medial Frontal Cortex Mediates Unconscious Inhibition of Voluntary Action , 2007, Neuron.

[19]  Peter Praamstra,et al.  The basal ganglia and inhibitory mechanisms in response selection: evidence from subliminal priming of motor responses in Parkinson's disease. , 2004, Brain : a journal of neurology.

[20]  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.

[21]  S. T. Klapp,et al.  Nonconscious control mimics a purposeful strategy: strength of Stroop-like interference is automatically modulated by proportion of compatible trials. , 2007, Journal of experimental psychology. Human perception and performance.

[22]  E. Maylor,et al.  No difference between conscious and nonconscious visuomotor control: Evidence from perceptual learning in the masked prime task , 2008, Consciousness and Cognition.

[23]  Borís Burle,et al.  Dynamics of facilitation and interference in cue-priming and Simon tasks , 2005 .

[24]  E. Maylor,et al.  Multiple systems for cognitive control: evidence from a hybrid prime-Simon task. , 2011, Journal of experimental psychology. Human perception and performance.

[25]  Derrick G. Watson,et al.  Aging and inhibitory processes in memory, attentional, and motor tasks , 2005 .

[26]  Cameron S. Carter,et al.  Conflict-related activity in the caudal anterior cingulate cortex in the absence of awareness , 2009, Biological Psychology.

[27]  R. Hyman Stimulus information as a determinant of reaction time. , 1953, Journal of experimental psychology.

[28]  T Hasbroucq,et al.  Cortico-spinal inhibition reflects time but not event preparation: neural mechanisms of preparation dissociated by transcranial magnetic stimulation. , 1999, Acta psychologica.

[29]  G. Gilmore,et al.  Age effects in coding tasks: componential analysis and test of the sensory deficit hypothesis. , 2006, Psychology and aging.

[30]  M. Eimer,et al.  Partial Response Activation to Masked Primes is Not Dependent on Response Readiness , 2001, Perceptual and motor skills.

[31]  L. Phillips,et al.  Differential Effects of Aging on Executive and Automatic Inhibition , 2008, Developmental neuropsychology.

[32]  P. Sumner,et al.  Oscillations in Motor Priming: Positive Rebound Follows the Inhibitory Phase in the Masked Prime Paradigm , 2008, Journal of motor behavior.

[33]  M. Leboyer,et al.  Conscious and subliminal conflicts in normal subjects and patients with schizophrenia: The role of the anterior cingulate , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[34]  James R. Tresilian,et al.  Continuous priming effects on discrete response choices , 2010, Brain and Cognition.

[35]  F. Collette,et al.  Inhibitory control of memory in normal ageing: Dissociation between impaired intentional and preserved unintentional processes , 2009, Memory.

[36]  T. Robbins,et al.  Inhibition of subliminally primed responses is mediated by the caudate and thalamus: evidence from functional MRI and Huntington's disease. , 2003, Brain : a journal of neurology.

[37]  John C. Rothwell,et al.  Age reduces cortical reciprocal inhibition in humans , 2006, Experimental Brain Research.

[38]  R. Verleger,et al.  Aging and the Simon task. , 2002, Psychophysiology.

[39]  Justin L. Vincent,et al.  Disruption of Large-Scale Brain Systems in Advanced Aging , 2007, Neuron.

[40]  Deana B. Davalos,et al.  Age differences in fluid intelligence: Contributions of general slowing and frontal decline , 2006, Brain and Cognition.

[41]  David L. Strayer,et al.  Aging and inhibition: beyond a unitary view of inhibitory processing in attention. , 1994, Psychology and aging.

[42]  E. Maylor,et al.  Motor control in old age: evidence of impaired low-level inhibition. , 2005, The journals of gerontology. Series B, Psychological sciences and social sciences.

[43]  J. Hoffmann,et al.  Mechanisms of subliminal response priming , 2008, Advances in cognitive psychology.

[44]  Jesse S. Husk,et al.  Age-related delay in information accrual for faces: Evidence from a parametric, single-trial EEG approach , 2010 .

[45]  P. Verhaeghen Aging and Executive Control: Reports of a Demise Greatly Exaggerated , 2011, Current directions in psychological science.

[46]  M. Eimer,et al.  Effects of masked stimuli on motor activation: behavioral and electrophysiological evidence. , 1998, Journal of experimental psychology. Human perception and performance.

[47]  S. Rombouts,et al.  Reduced resting-state brain activity in the "default network" in normal aging. , 2008, Cerebral cortex.

[48]  J. Rothwell,et al.  The effect of age on task-related modulation of interhemispheric balance , 2007, Experimental Brain Research.

[49]  Stewart H. Mostofsky,et al.  Response Inhibition and Response Selection: Two Sides of the Same Coin , 2008, Journal of Cognitive Neuroscience.

[50]  J. Duncan,et al.  Filtering of neural signals by focused attention in the monkey prefrontal cortex , 2002, Nature Neuroscience.

[51]  Diane Swick,et al.  Are the neural correlates of stopping and not going identical? Quantitative meta-analysis of two response inhibition tasks , 2011, NeuroImage.

[52]  Petroc Sumner,et al.  Automatic motor activation in the executive control of action , 2012, Front. Hum. Neurosci..

[53]  M. Eimer,et al.  The Influence of Subliminally Presented Primes on Response Preparation , 1997 .

[54]  H. Bowman,et al.  Dissociating local and global levels of perceptuo-motor control in masked priming. , 2006, Journal of experimental psychology. Human perception and performance.

[55]  J. Nigg On inhibition/disinhibition in developmental psychopathology: views from cognitive and personality psychology and a working inhibition taxonomy. , 2000, Psychological bulletin.

[56]  Franck Vidal,et al.  Physiological evidence for response inhibition in choice reaction time tasks , 2004, Brain and Cognition.

[57]  D. Wechsler Manual for the Wechsler Adult Intelligence Scale. , 1955 .

[58]  E. Maylor,et al.  Age-related deficits in low-level inhibitory motor control. , 2011, Psychology and aging.

[59]  Julie Duque,et al.  Behavioral / Systems / Cognitive Evidence for Two Concurrent Inhibitory Mechanisms during Response Preparation , 2010 .

[60]  C Meinecke,et al.  Learning to ignore the mask in texture segmentation tasks. , 2001, Journal of experimental psychology. Human perception and performance.

[61]  Martin Eimer,et al.  Links between conscious awareness and response inhibition: Evidence from masked priming , 2002, Psychonomic bulletin & review.

[62]  P. Rabbitt,et al.  Contribution of cognitive abilities to performance and improvement on a substitution coding task. , 1999, Psychology and aging.

[63]  David M. Lane,et al.  Information processing components of substitution test performance. , 1985 .

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