Brain activation during associative short-term memory maintenance is not predictive for subsequent retrieval

Performance on working memory (WM) tasks may partially be supported by long-term memory (LTM) processing. Hence, brain activation recently being implicated in WM may actually have been driven by (incidental) LTM formation. We examined which brain regions actually support successful WM processing, rather than being confounded by LTM processes, during the maintenance and probe phase of a WM task. We administered a four-pair (faces and houses) associative delayed-match-to-sample (WM) task using event-related functional MRI (fMRI) and a subsequent associative recognition LTM task, using the same stimuli. This enabled us to analyze subsequent memory effects for both the WM and the LTM test by contrasting correctly recognized pairs with incorrect pairs for either task. Critically, with respect to the subsequent WM effect, we computed this analysis exclusively for trials that were forgotten in the subsequent LTM recognition task. Hence, brain activity associated with successful WM processing was less likely to be confounded by incidental LTM formation. The subsequent LTM effect, in contrast, was analyzed exclusively for pairs that previously had been correctly recognized in the WM task, disclosing brain regions involved in successful LTM formation after successful WM processing. Results for the subsequent WM effect showed no significantly activated brain areas for WM maintenance, possibly due to an insensitivity of fMRI to mechanisms underlying active WM maintenance. In contrast, a correct decision at WM probe was linked to activation in the “retrieval success network” (anterior and posterior midline brain structures). The subsequent LTM analyses revealed greater activation in left dorsolateral prefrontal cortex and posterior parietal cortex in the early phase of the maintenance stage. No supra-threshold activation was found during the WM probe. Together, we obtained clearer insights in which brain regions support successful WM and LTM without the potential confound of the respective memory system.

[1]  J. D. E. Gabrieli,et al.  Integration of diverse information in working memory within the frontal lobe , 2000, Nature Neuroscience.

[2]  Nikolai Axmacher,et al.  Interaction of working memory and long-term memory in the medial temporal lobe. , 2008, Cerebral cortex.

[3]  Hilla Peretz,et al.  Ju n 20 03 Schrödinger ’ s Cat : The rules of engagement , 2003 .

[4]  R. Kessels,et al.  Spatial and non-spatial contextual working memory in patients with diencephalic or hippocampal dysfunction , 2007, Brain Research.

[5]  John D E Gabrieli,et al.  Working memory and long‐term memory for faces: Evidence from fMRI and global amnesia for involvement of the medial temporal lobes , 2006, Hippocampus.

[6]  C. Ranganath.  Working memory for visual objects: Complementary roles of inferior temporal, medial temporal, and prefrontal cortex , 2006, Neuroscience.

[7]  F. Craik.  Levels of processing: Past, present... and future? , 2002, Memory.

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

[9]  Ellen M. Migo,et al.  Associative memory and the medial temporal lobes , 2007, Trends in Cognitive Sciences.

[10]  Nikolai Axmacher,et al.  Electrophysiological signature of working and long‐term memory interaction in the human hippocampus , 2010, The European journal of neuroscience.

[11]  N. Cohen,et al.  Relational Memory and the Hippocampus: Representations and Methods , 2009, Front. Neurosci..

[12]  A. Baddeley.  Working memory: theories, models, and controversies. , 2012, Annual review of psychology.

[13]  N. Cowan.  An embedded-processes model of working memory , 1999 .

[14]  Ingrid R. Olson,et al.  Working Memory for Conjunctions Relies on the Medial Temporal Lobe , 2006, The Journal of Neuroscience.

[15]  J. Knierim.  The hippocampus , 2015, Current Biology.

[16]  Charan Ranganath,et al.  Opinion TRENDS in Cognitive Sciences Vol.9 No.8 August 2005 Doubts about double dissociations between short- and long-term memory , 2022 .

[17]  L. Squire,et al.  Working memory, long-term memory, and medial temporal lobe function. , 2011, Learning & memory.

[18]  M. D’Esposito,et al.  Functional connectivity during working memory maintenance , 2004, Cognitive, affective & behavioral neuroscience.

[19]  Anjan Chatterjee,et al.  Visual Working Memory Is Impaired when the Medial Temporal Lobe Is Damaged , 2006, Journal of Cognitive Neuroscience.

[20]  Bradley R. Postle,et al.  Activation and Information in Working Memory Research , 2015 .

[21]  Karl J. Friston,et al.  A unified statistical approach for determining significant signals in images of cerebral activation , 1996, Human brain mapping.

[22]  F. Rösler,et al.  Theta and alpha oscillations during working-memory maintenance predict successful long-term memory encoding , 2010, Neuroscience Letters.

[23]  Frank Rösler,et al.  Working memory maintenance contributes to long-term memory formation: Evidence from slow event-related brain potentials , 2007, Cognitive, affective & behavioral neuroscience.

[24]  John D E Gabrieli,et al.  Performance-Related Sustained and Anticipatory Activity in Human Medial Temporal Lobe during Delayed Match-to-Sample , 2009, The Journal of Neuroscience.

[25]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[26]  Morris Moscovitch,et al.  Neuroimaging the Serial Position Curve , 2005, Psychological science.

[27]  A. Baddeley,et al.  Amnesia and the distinction between long- and short-term memory. , 1970 .

[28]  A. Miyake,et al.  Models of Working Memory: Mechanisms of Active Maintenance and Executive Control , 1999 .

[29]  D. Schacter,et al.  Prefrontal Contributions to Executive Control: fMRI Evidence for Functional Distinctions within Lateral Prefrontal Cortex , 2001, NeuroImage.

[30]  Guillén Fernández,et al.  Distinct neural correlates of associative working memory and long-term memory encoding in the medial temporal lobe , 2012, NeuroImage.

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

[32]  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.

[33]  Donna Rose Addis,et al.  The Wiley Handbook on The Cognitive Neuroscience of Memory , 2015 .

[34]  Craig J. Brozinsky,et al.  Lag‐sensitive repetition suppression effects in the anterior parahippocampal gyrus , 2005, Hippocampus.

[35]  C. Jacobsen.  FUNCTIONS OF FRONTAL ASSOCIATION AREA IN PRIMATES , 1935 .

[36]  C. Pennartz,et al.  Dissociating the “retrieval success” regions of the brain: Effects of retrieval delay , 2010, Neuropsychologia.

[37]  Marian E. Berryhill,et al.  Insights from neuropsychology: pinpointing the role of the posterior parietal cortex in episodic and working memory , 2012, Front. Integr. Neurosci..

[38]  K. Maccorquodale.  Organization of Behavior : A Neuropsychological Theory , 1951 .

[39]  F. Craik,et al.  The role of rehearsal in short-term memory , 1973 .

[40]  Clayton E. Curtis,et al.  Maintenance of Spatial and Motor Codes during Oculomotor Delayed Response Tasks , 2004, The Journal of Neuroscience.

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

[42]  O. Jensen,et al.  Maintenance of multiple working memory items by temporal segmentation , 2006, Neuroscience.

[43]  R. Andersen,et al.  Memory related motor planning activity in posterior parietal cortex of macaque , 1988, Experimental Brain Research.

[44]  M. Leszczyński.  How Does Hippocampus Contribute to Working Memory Processing? , 2011, Front. Hum. Neurosci..

[45]  Jarrod A. Lewis-Peacock,et al.  Multiple neural states of representation in short-term memory? It’s a matter of attention , 2014, Front. Hum. Neurosci..

[46]  K. Henke.  A model for memory systems based on processing modes rather than consciousness , 2010, Nature Reviews Neuroscience.

[47]  John Jonides,et al.  Maintenance rehearsal: a two-component analysis , 1984 .

[48]  Michael X. Cohen,et al.  Sustained Neural Activity Patterns during Working Memory in the Human Medial Temporal Lobe , 2007, The Journal of Neuroscience.

[49]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[50]  B. Milner,et al.  What went where? Impaired object‐location learning in patients with right hippocampal lesions , 2005, Hippocampus.

[51]  C Caltagirone,et al.  Parieto-frontal interactions in visual-object and visual-spatial working memory: evidence from transcranial magnetic stimulation. , 2001, Cerebral cortex.

[52]  Lila Davachi,et al.  When Keeping in Mind Supports Later Bringing to Mind: Neural Markers of Phonological Rehearsal Predict Subsequent Remembering , 2001, Journal of Cognitive Neuroscience.

[53]  T. Shallice,et al.  Please Scroll down for Article the Quarterly Journal of Experimental Psychology Independent Functioning of Verbal Memory Stores: a Neuropsychological Study Independent Functioning of Verbal Memory Stores : a Neuropsychological Study , 2022 .

[54]  Neal J. Cohen,et al.  The Long and the Short of It: Relational Memory Impairments in Amnesia, Even at Short Lags , 2006, The Journal of Neuroscience.

[55]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[56]  Lila Davachi,et al.  Working Memory Retrieval: Contributions of the Left Prefrontal Cortex, the Left Posterior Parietal Cortex, and the Hippocampus , 2009, Journal of Cognitive Neuroscience.

[57]  J. Fell,et al.  Cross-frequency coupling supports multi-item working memory in the human hippocampus , 2010, Proceedings of the National Academy of Sciences.

[58]  Guillén Fernández,et al.  The right hippocampus participates in short-term memory maintenance of object–location associations , 2006, NeuroImage.

[59]  N. Burgess,et al.  The hippocampus is required for short‐term topographical memory in humans , 2007, Hippocampus.

[60]  C. Stark,et al.  Medial temporal lobe activation during encoding and retrieval of novel face-name pairs , 2004, Hippocampus.

[61]  Guillén Fernández,et al.  The hippocampus supports encoding of between-domain associations within working memory. , 2009, Learning & memory.

[62]  J. Fuster,et al.  Unit activity in monkey parietal cortex related to haptic perception and temporary memory , 2004, Experimental Brain Research.

[63]  D. Amaral,et al.  Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents , 1994, The Journal of comparative neurology.

[64]  W. Singer,et al.  Dynamic predictions: Oscillations and synchrony in top–down processing , 2001, Nature Reviews Neuroscience.

[65]  Marcia K. Johnson,et al.  fMRI evidence of age-related hippocampal dysfunction in feature binding in working memory. , 2000, Brain research. Cognitive brain research.

[66]  J. Fell,et al.  The role of phase synchronization in memory processes , 2011, Nature Reviews Neuroscience.

[67]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[68]  B. Postle,et al.  Maintenance versus Manipulation of Information Held in Working Memory: An Event-Related fMRI Study , 1999, Brain and Cognition.

[69]  Rosanna K. Olsen,et al.  Working memory and amnesia: The role of stimulus novelty , 2012, Neuropsychologia.

[70]  Benjamin J. Shannon,et al.  Parietal lobe contributions to episodic memory retrieval , 2005, Trends in Cognitive Sciences.

[71]  Mieke Verfaellie,et al.  Disproportionate deficit in associative recognition relative to item recognition in global amnesia , 2003, Cognitive, affective & behavioral neuroscience.

[72]  L. Nadel,et al.  Update on Memory Systems and Processes , 2011, Neuropsychopharmacology.

[73]  J. Fuster.  Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. , 1973, Journal of neurophysiology.

[74]  J. Aggleton,et al.  The performance of amnesic subjects on tests of delayed matching-to-sample and delayed matching-to-position , 1995, Neuropsychologia.

[75]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[76]  John K. Tsotsos,et al.  Direct neurophysiological evidence for spatial suppression surrounding the focus of attention in vision. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[77]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

[78]  P. Goldman-Rakic,et al.  Delay-related activity of prefrontal neurons in rhesus monkeys performing delayed response , 1982, Brain Research.

[79]  Michael X. Cohen,et al.  Interference of working memory load with long‐term memory formation , 2009, The European journal of neuroscience.

[80]  John Kounios,et al.  Coherent oscillatory networks supporting short-term memory retention , 2009, Brain Research.

[81]  R. Logie,et al.  Neural correlates of shape–color binding in visual working memory , 2014, Neuropsychologia.

[82]  N. Cashdollar,et al.  Hippocampus-dependent and -independent theta-networks of active maintenance , 2009, Proceedings of the National Academy of Sciences.

[83]  R. Berndt,et al.  Working memory retention systems: a state of activated long-term memory. , 2003, The Behavioral and brain sciences.

[84]  M. O. Olde Rikkert,et al.  Working memory binding and episodic memory formation in aging, mild cognitive impairment, and Alzheimer’s dementia , 2015, Journal of clinical and experimental neuropsychology.

[85]  Lily Riggs,et al.  The hippocampus supports multiple cognitive processes through relational binding and comparison , 2012, Front. Hum. Neurosci..

[86]  Charan Ranganath,et al.  Medial Temporal Lobe Coding of Item and Spatial Information during Relational Binding in Working Memory , 2014, The Journal of Neuroscience.

[87]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[88]  Richard L. Lewis,et al.  The mind and brain of short-term memory. , 2008, Annual review of psychology.

[89]  Albert Postma,et al.  Frontal-Lobe Involvement in Spatial Memory: Evidence from PET, fMRI, and Lesion Studies , 2000, Neuropsychology Review.

[90]  J. Knott.  The organization of behavior: A neuropsychological theory , 1951 .

[91]  David Luck,et al.  The right parahippocampal gyrus contributes to the formation and maintenance of bound information in working memory , 2010, Brain and Cognition.

[92]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[93]  J. Lisman,et al.  Hippocampal sequence-encoding driven by a cortical multi-item working memory buffer , 2005, Trends in Neurosciences.

[94]  Rodrigo F. Salazar,et al.  Content-Specific Fronto-Parietal Synchronization During Visual Working Memory , 2012, Science.

[95]  M. Hasselmo,et al.  Greater working memory load results in greater medial temporal activity at retrieval. , 2009, Cerebral cortex.

[96]  Charan Ranganath,et al.  Medial Temporal Lobe Activity Predicts Successful Relational Memory Binding , 2008, The Journal of Neuroscience.

[97]  Michael X. Cohen,et al.  Working Memory Maintenance Contributes to Long-term Memory Formation: Neural and Behavioral Evidence , 2005, Journal of Cognitive Neuroscience.

[98]  R. Kessels,et al.  Different types of working memory binding in epilepsy patients with unilateral anterior temporal lobectomy , 2014, Brain and Cognition.

[99]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]／Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[100]  Guillén Fernández,et al.  Early and late stages of working-memory maintenance contribute differentially to long-term memory formation. , 2013, Acta psychologica.

[101]  Michael D. Rugg,et al.  Further Dissociating the Processes Involved in Recognition Memory: An fMRI Study , 2005, Journal of Cognitive Neuroscience.

[102]  R. Kessels,et al.  Dissociating the Neural Correlates of Intra-Item and Inter-Item Working-Memory Binding , 2010, PloS one.