Interference Control in Working Memory Is Associated with Ventrolateral Prefrontal Cortex Volume

Goal-irrelevant information may interfere with ongoing task activities if not controlled properly. Evidence suggests that the ability to control interference is connected mainly to the prefrontal cortex (pFC). However, it remains unclear whether gray matter (GM) volume in prefrontal regions influences individual differences in interference control (IC) and if these relationships are affected by aging. Using cross-sectional and longitudinal estimates over a 4- to 5-year period, we examined the relationship between relative IC scores, obtained from a 2-back working memory task, GM volumes, and performance in different cognitive domains. By identifying individuals with either no or high levels of interference, we demonstrated that participants with superior IC had larger volume of the ventrolateral pFC, regardless of participant demographics. The same pattern was observed both at baseline and follow-up. Cross-sectional estimates further showed that interference increased as a function of age, but interference did not change between baseline and follow-up. Similarly, across-sample associations between IC and pFC volume were found in the cross-sectional data, along with no longitudinal change–change relationships. Moreover, relative IC scores could be linked to composite scores of fluid intelligence, indicating that control of interference may relate to performance in expected cognitive domains. These results provide new evidence that a relative IC score can be related to volume of specific and relevant regions within pFC and that this relationship is not modulated by age. This supports a view that the GM volume in these regions plays a role in resisting interference during a working memory task.

[1]  Stephan Lewandowsky,et al.  Working memory updating involves item-specific removal , 2014 .

[2]  Richard L. Lewis,et al.  Resolving semantic and proactive interference in memory over the short-term , 2011, Memory & cognition.

[3]  R. N. Spreng,et al.  Executive functions and neurocognitive aging: dissociable patterns of brain activity , 2012, Neurobiology of Aging.

[4]  S. Eickhoff,et al.  Neuroscience and Biobehavioral Reviews Three Key Regions for Supervisory Attentional Control: Evidence from Neuroimaging Meta-analyses , 2022 .

[5]  Jonas Persson,et al.  Context-dependent switching between proactive and reactive working memory control mechanisms in the right inferior frontal gyrus , 2012, NeuroImage.

[6]  Tor D. Wager,et al.  Common and unique components of response inhibition revealed by fMRI , 2005, NeuroImage.

[7]  Shu-Chen Li,et al.  Interference and facilitation in spatial working memory: age-associated differences in lure effects in the n-back paradigm. , 2009, Psychology and aging.

[8]  Robert Leech,et al.  Network mechanisms of intentional learning , 2016, NeuroImage.

[9]  Ullrich K. H. Ecker,et al.  Removal of information from working memory: A specific updating process , 2014 .

[10]  Cynthia P. May,et al.  Inhibitory control over no-longer-relevant information: Adult age differences , 1997, Memory & cognition.

[11]  Anders M. Dale,et al.  Six-month atrophy in MTL structures is associated with subsequent memory decline in elderly controls , 2010, NeuroImage.

[12]  Marcia K. Johnson,et al.  Source monitoring 15 years later: what have we learned from fMRI about the neural mechanisms of source memory? , 2009, Psychological bulletin.

[13]  L. Nyberg,et al.  Memory aging and brain maintenance , 2012, Trends in Cognitive Sciences.

[14]  S. Resnick,et al.  Differential trajectories of age-related changes in components of executive and memory processes. , 2012, Psychology and aging.

[15]  T. Robbins,et al.  Dissociating Inhibition, Attention, and Response Control in the Frontoparietal Network Using Functional Magnetic Resonance Imaging , 2010, Cerebral cortex.

[16]  L. Nyberg,et al.  The betula prospective cohort study: Memory, health, and aging , 1997 .

[17]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

[18]  E E Smith,et al.  The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[19]  David Badre,et al.  Left ventrolateral prefrontal cortex and the cognitive control of memory , 2007, Neuropsychologia.

[20]  C Brock Kirwan,et al.  Overcoming interference: an fMRI investigation of pattern separation in the medial temporal lobe. , 2007, Learning & memory.

[21]  Sebastian Schneegans,et al.  Neural Architecture for Feature Binding in Visual Working Memory , 2017, The Journal of Neuroscience.

[22]  Kathryn M. McMillan,et al.  N‐back working memory paradigm: A meta‐analysis of normative functional neuroimaging studies , 2005, Human brain mapping.

[23]  Adam J. Woods,et al.  Frontal Structural Neural Correlates of Working Memory Performance in Older Adults , 2017, Front. Aging Neurosci..

[24]  A. Lundervold,et al.  Salient measures of inhibition and switching are associated with frontal lobe gray matter volume in healthy middle-aged and older adults. , 2014, Neuropsychology.

[25]  Susanne M. Jaeggi,et al.  A common neural hub resolves syntactic and non-syntactic conflict through cooperation with task-specific networks , 2017, Brain and Language.

[26]  Bruce Fischl,et al.  Within-subject template estimation for unbiased longitudinal image analysis , 2012, NeuroImage.

[27]  Michael W Weiner,et al.  Longitudinal MRI and cognitive change in healthy elderly. , 2007, Neuropsychology.

[28]  Jonas Persson,et al.  Differential Effects of Encoding Instructions on Brain Activity Patterns of Item and Associative Memory , 2017, Journal of Cognitive Neuroscience.

[29]  L. Jäncke,et al.  Brain size, sex, and the aging brain , 2015, Human brain mapping.

[30]  P. Rabbitt,et al.  Two thirds of the age-based changes in fluid and crystallized intelligence, perceptual speed, and memory in adulthood are shared , 2012 .

[31]  K. Warner Schaie,et al.  Developmental Influences on Adult Intelligence: The Seattle Longitudinal Study , 2012 .

[32]  Andrew R. A. Conway,et al.  Journal of Experimental Psychology : General Neural Mechanisms of Interference Control Underlie the Relationship Between Fluid Intelligence and Working Memory Span , 2011 .

[33]  J. Alvarez,et al.  Executive Function and the Frontal Lobes: A Meta-Analytic Review , 2006, Neuropsychology Review.

[34]  Pamela K. Smith,et al.  Models of visuospatial and verbal memory across the adult life span. , 2002, Psychology and aging.

[35]  Daniel L. Schacter,et al.  Intrinsic Architecture Underlying the Relations among the Default, Dorsal Attention, and Frontoparietal Control Networks of the Human Brain , 2013, Journal of Cognitive Neuroscience.

[36]  W. Revelle psych: Procedures for Personality and Psychological Research , 2017 .

[37]  R. Poldrack,et al.  Dissociable Controlled Retrieval and Generalized Selection Mechanisms in Ventrolateral Prefrontal Cortex , 2005, Neuron.

[38]  J. Jonides,et al.  Brain mechanisms of proactive interference in working memory , 2006, Neuroscience.

[39]  Charan Ranganath,et al.  Prefrontal Cortex and Long-Term Memory Encoding: An Integrative Review of Findings from Neuropsychology and Neuroimaging , 2007, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[40]  David Badre,et al.  Frontal lobe mechanisms that resolve proactive interference. , 2005, Cerebral cortex.

[41]  D. Jeste,et al.  A review of the brain structure correlates of successful cognitive aging. , 2011, The Journal of neuropsychiatry and clinical neurosciences.

[42]  C. Studholme,et al.  Brain atrophy associated with baseline and longitudinal measures of cognition , 2011, Neurobiology of Aging.

[43]  Ulman Lindenberger,et al.  Trajectories of brain aging in middle-aged and older adults: Regional and individual differences , 2010, NeuroImage.

[44]  L Penke,et al.  Childhood cognitive ability accounts for associations between cognitive ability and brain cortical thickness in old age , 2013, Molecular Psychiatry.

[45]  J. McCabe,et al.  Working Memory for Item and Temporal Information in Younger and Older Adults , 2008, Neuropsychology, development, and cognition. Section B, Aging, neuropsychology and cognition.

[46]  N. Schuff,et al.  Longitudinal volumetric MRI change and rate of cognitive decline , 2005, Neurology.

[47]  Lynn Hasher,et al.  Working Memory and Aging: Current Status of the Inhibitory View , 1996 .

[48]  Joshua W. Brown,et al.  A meta-analysis of executive components of working memory. , 2013, Cerebral cortex.

[49]  Donald T Stuss,et al.  Functions of the Frontal Lobes: Relation to Executive Functions , 2011, Journal of the International Neuropsychological Society.

[50]  T. Salthouse Frequent assessments may obscure cognitive decline. , 2014, Psychological assessment.

[51]  J. Duncan,et al.  Common regions of the human frontal lobe recruited by diverse cognitive demands , 2000, Trends in Neurosciences.

[52]  Yang Yang,et al.  Neural Systems Underlying Emotional and Non-emotional Interference Processing: An ALE Meta-Analysis of Functional Neuroimaging Studies , 2016, Front. Behav. Neurosci..

[53]  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.

[54]  J. Gabrieli,et al.  Immature Frontal Lobe Contributions to Cognitive Control in Children Evidence from fMRI , 2002, Neuron.

[55]  J. Jonides,et al.  Interference resolution: Insights from a meta-analysis of neuroimaging tasks , 2007, Cognitive, affective & behavioral neuroscience.

[56]  Faith M. Gunning-Dixon,et al.  Neuroanatomical correlates of selected executive functions in middle-aged and older adults: a prospective MRI study , 2003, Neuropsychologia.

[57]  C. Chabris,et al.  Neural mechanisms of general fluid intelligence , 2003, Nature Neuroscience.

[58]  John Jonides,et al.  Common and distinct neural correlates of perceptual and memorial selection , 2009, NeuroImage.

[59]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[60]  L. Bäckman,et al.  Age-Differences in the Temporal Properties of Proactive Interference in Working Memory , 2017, Psychology and aging.

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

[62]  S. Jaeggi,et al.  The concurrent validity of the N-back task as a working memory measure , 2010, Memory.

[63]  Jonas Persson,et al.  Mapping interference resolution across task domains: A shared control process in left inferior frontal gyrus , 2009, Brain Research.

[64]  A. Miyake,et al.  The relations among inhibition and interference control functions: a latent-variable analysis. , 2004, Journal of experimental psychology. General.

[65]  C. Ranganath,et al.  The Dorsolateral Prefrontal Cortex Contributes to Successful Relational Memory Encoding , 2007, The Journal of Neuroscience.

[66]  John Jonides,et al.  Order Information in Working Memory: fMRI Evidence for Parietal and Prefrontal Mechanisms , 2000, Journal of Cognitive Neuroscience.

[67]  R. Buckner Memory and Executive Function in Aging and AD Multiple Factors that Cause Decline and Reserve Factors that Compensate , 2004, Neuron.

[68]  Robert T. Knight,et al.  Effects of frontal lobe damage on interference effects in working memory , 2002, Cognitive, affective & behavioral neuroscience.

[69]  Paul Verhaeghen,et al.  Age-related differences in control processes in verbal and visuospatial working memory: storage, transformation, supervision, and coordination. , 2007, The journals of gerontology. Series B, Psychological sciences and social sciences.

[70]  Tobias Egner,et al.  An insula-frontostriatal network mediates flexible cognitive control by adaptively predicting changing control demands , 2015, Nature Communications.

[71]  L Hasher,et al.  Working memory span and the role of proactive interference. , 2001, Journal of experimental psychology. General.

[72]  Lesley K. Fellows,et al.  Lesion Evidence That Two Distinct Regions within Prefrontal Cortex are Critical for n-Back Performance in Humans , 2009, Journal of Cognitive Neuroscience.

[73]  K. Oberauer Removing irrelevant information from working memory: a cognitive aging study with the modified Sternberg task. , 2001, Journal of experimental psychology. Learning, memory, and cognition.

[74]  Brenda A. Kirchhoff,et al.  Left caudal middle frontal gray matter volume mediates the effect of age on self-initiated elaborative encoding strategies , 2017, Neuropsychologia.

[75]  T. Robbins,et al.  Evidence Supports Specific Braking Function for Inferior PFC , 2015, Trends in Cognitive Sciences.

[76]  D. Sharp,et al.  Contrasting network and modular perspectives on inhibitory control , 2015, Trends in Cognitive Sciences.

[77]  Thomas S. Redick,et al.  Complex span and n-back measures of working memory: A meta-analysis , 2013, Psychonomic bulletin & review.

[78]  Alice J. Corkill,et al.  Individual differences in susceptibility to interference and general cognitive ability , 1999 .

[79]  Michael R. Dulas,et al.  Age-related changes in overcoming proactive interference in associative memory: The role of PFC-mediated executive control processes at retrieval , 2016, NeuroImage.

[80]  M. Naveh-Benjamin Adult age differences in memory performance: tests of an associative deficit hypothesis. , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[81]  Donna Rose Addis,et al.  Prefrontal and hippocampal contributions to the generation and binding of semantic associations during successful encoding , 2006, NeuroImage.

[82]  Anand R. Kumar,et al.  Executive function and MRI prefrontal volumes among healthy older adults. , 2008, Neuropsychology.

[83]  K. Oberauer Binding and inhibition in working memory: individual and age differences in short-term recognition. , 2005, Journal of experimental psychology. General.

[84]  Randi C. Martin,et al.  Dissociations among tasks involving inhibition: A single-case study , 2005, Cognitive, affective & behavioral neuroscience.

[85]  Richard P. Heitz,et al.  The speed-accuracy tradeoff: history, physiology, methodology, and behavior , 2014, Front. Neurosci..

[86]  Peng Yuan,et al.  Fluid intelligence and gross structural properties of the cerebral cortex in middle-aged and older adults: A multi-occasion longitudinal study , 2018, NeuroImage.

[87]  Jonas Persson,et al.  Imaging Fatigue of Interference Control Reveals the Neural Basis of Executive Resource Depletion , 2013, Journal of Cognitive Neuroscience.

[88]  Audrey Duarte,et al.  The effects of aging on material-independent and material-dependent neural correlates of source memory retrieval. , 2012, Cerebral cortex.

[89]  A. Miyake,et al.  Unity and diversity of executive functions: Individual differences as a window on cognitive structure , 2017, Cortex.

[90]  T. Salthouse Effects of first occasion test experience on longitudinal cognitive change. , 2013, Developmental psychology.

[91]  Marcia K. Johnson,et al.  Feature memory and binding in young and older adults , 1996, Memory & cognition.

[92]  T. Salthouse When does age-related cognitive decline begin? , 2009, Neurobiology of Aging.

[93]  Adam Hampshire,et al.  Putting the brakes on inhibitory models of frontal lobe function , 2015, NeuroImage.

[94]  Trey Hedden,et al.  Contributions of source and inhibitory mechanisms to age-related retroactive interference in verbal working memory. , 2003, Journal of experimental psychology. General.

[95]  Jonas Persson,et al.  Longitudinal structure-function correlates in elderly reveal MTL dysfunction with cognitive decline. , 2012, Cerebral cortex.

[96]  Michael F. Bunting,et al.  Proactive interference and item similarity in working memory. , 2006, Journal of experimental psychology. Learning, memory, and cognition.

[97]  M. D’Esposito Working memory. , 2008, Handbook of clinical neurology.

[98]  C. Lustig,et al.  Inhibitory Mechanisms and the Control of Attention , 2007 .

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

[100]  Klaus Oberauer,et al.  An Interference Model of Visual Working Memory , 2017, Psychological review.

[101]  J. Desmond,et al.  Prefrontal regions involved in keeping information in and out of mind. , 2001, Brain : a journal of neurology.

[102]  Adam Gazzaley,et al.  A cognitive framework for understanding and improving interference resolution in the brain. , 2013, Progress in brain research.

[103]  Jonathan D. Power,et al.  Multi-task connectivity reveals flexible hubs for adaptive task control , 2013, Nature Neuroscience.

[104]  Robert Leech,et al.  Dynamic Network Mechanisms of Relational Integration , 2015, The Journal of Neuroscience.

[105]  T. Salthouse,et al.  Effects of increased processing demands on age differences in working memory. , 1990, Psychology and aging.

[106]  Michael W. L. Chee,et al.  Longitudinal brain structure and cognitive changes over 8 years in an East Asian cohort , 2017, NeuroImage.

[107]  L. Nyberg,et al.  Longitudinal association between hippocampus atrophy and episodic-memory decline , 2017, Neurobiology of Aging.

[108]  Lynn Hasher,et al.  The role of interference in memory span , 1999, Memory & cognition.

[109]  Y. Miyashita,et al.  Preparation to Inhibit a Response Complements Response Inhibition during Performance of a Stop-Signal Task , 2009, The Journal of Neuroscience.

[110]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[111]  A. Dale,et al.  Whole Brain Segmentation Automated Labeling of Neuroanatomical Structures in the Human Brain , 2002, Neuron.

[112]  R. Engle,et al.  Working Memory Capacity and Fluid Intelligence , 2016, Perspectives on psychological science : a journal of the Association for Psychological Science.

[113]  N. Raz,et al.  Prefrontal cortex and executive functions in healthy adults: A meta-analysis of structural neuroimaging studies , 2014, Neuroscience & Biobehavioral Reviews.

[114]  James B. Brewer,et al.  Dissociation of Frontal and Medial Temporal Lobe Activity in Maintenance and Binding of Sequentially Presented Paired Associates , 2009, Journal of Cognitive Neuroscience.

[115]  Robert H. Paul,et al.  The relationship between frontal gray matter volume and cognition varies across the healthy adult lifespan. , 2006, The American journal of geriatric psychiatry : official journal of the American Association for Geriatric Psychiatry.

[116]  Angela R. Laird,et al.  Modelling neural correlates of working memory: A coordinate-based meta-analysis , 2012, NeuroImage.