Long-term effects of interference on short-term memory performance in the rat

A distinction has always been made between long-term and short-term memory (also now called working memory, WM). The obvious difference between these two kinds of memory concerns the duration of information storage: information is supposedly transiently stored in WM while it is considered durably consolidated into long-term memory. It is well acknowledged that the content of WM is erased and reset after a short time, to prevent irrelevant information from proactively interfering with newly stored information. In the present study, we used typical WM radial maze tasks to question the brief lifespan of spatial WM content in rodents. Groups of rats were submitted to one of two different WM tasks in a radial maze: a WM task involving the repetitive presentation of a same pair of arms expected to induce a high level of proactive interference (PI) (HIWM task), or a task using a different pair in each trial expected to induce a low level of PI (LIWM task). Performance was effectively lower in the HIWM group than in LIWM in the final trial of each training session, indicative of a “within-session/short-term” PI effect. However, we also observed a different “between-session/long-term” PI effect between the two groups: while performance of LIWM trained rats remained stable over days, the performance of HIWM rats dropped after 10 days of training, and this impairment was visible from the very first trial of the day, hence not attributable to within-session PI. We also showed that a 24 hour-gap across training sessions known to allow consolidation processes to unfold, was a necessary and sufficient condition for the long-term PI effect to occur. These findings suggest that in the HIWM task, WM content was not entirely reset between training sessions and that, in specific conditions, WM content can outlast its purpose by being stored more permanently, generating a long-term deleterious effect of PI. The alternative explanation is that WM content could be transferred and stored more permanently in an intermediary form or memory between WM and long-term memory.

[1]  N. Cowan.  What are the differences between long-term, short-term, and working memory? , 2008, Progress in brain research.

[2]  C. Beaman,et al.  Working memory and working attention : What could possibly evolve ? , 2015 .

[3]  N. Cowan.  The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[4]  Richard C. Atkinson,et al.  Human Memory: A Proposed System and its Control Processes , 1968, Psychology of Learning and Motivation.

[5]  W. Ma,et al.  Changing concepts of working memory , 2014, Nature Neuroscience.

[6]  B. Underwood.  Interference and forgetting. , 1957, Psychological review.

[7]  J M Fuster,et al.  Memory in the cortex of the primate. , 1995, Biological research.

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

[9]  Hermann Ebbinghaus (1885).  Memory: A Contribution to Experimental Psychology , 2013, Annals of Neurosciences.

[10]  Ovid J. L. Tzeng,et al.  A study-phase retrieval model of temporal coding. , 1980 .

[11]  James J. Knierim,et al.  Tracking the flow of hippocampal computation: Pattern separation, pattern completion, and attractor dynamics , 2016, Neurobiology of Learning and Memory.

[12]  A. Fenton,et al.  Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation , 2011, Nature.

[13]  S. Becker.  A computational principle for hippocampal learning and neurogenesis , 2005, Hippocampus.

[14]  B. Bontempi,et al.  Time-dependent reorganization of brain circuitry underlying long-term memory storage , 1999, Nature.

[15]  G. A. Miller.  THE PSYCHOLOGICAL REVIEW THE MAGICAL NUMBER SEVEN, PLUS OR MINUS TWO: SOME LIMITS ON OUR CAPACITY FOR PROCESSING INFORMATION 1 , 1956 .

[16]  C. Degueldre,et al.  Are Spatial Memories Strengthened in the Human Hippocampus during Slow Wave Sleep? , 2004, Neuron.

[17]  R. Dale,et al.  Remembrance of places lasts: Proactive inhibition and patterns of choice in rat spatial memory , 1981 .

[18]  Paul Antoine Salin,et al.  Differential changes in hippocampal CaMKII and GluA1 activity after memory training involving different levels of adaptive forgetting , 2017, Learning & memory.

[19]  J. Born,et al.  About sleep's role in memory. , 2013, Physiological reviews.

[20]  C. Stark,et al.  Pattern separation in the hippocampus , 2011, Trends in Neurosciences.

[21]  Paul Smolen,et al.  The right time to learn: mechanisms and optimization of spaced learning , 2016, Nature Reviews Neuroscience.

[22]  J A Nevin,et al.  Acquisition of delayed matching in the pigeon. , 1963, Journal of the experimental analysis of behavior.

[23]  A. Battersby.  Plans and the Structure of Behavior , 1968 .

[24]  Eric R. Kandel,et al.  Inducible and Reversible Enhancement of Learning, Memory, and Long-Term Potentiation by Genetic Inhibition of Calcineurin , 2001, Cell.

[25]  Stefano Fusi,et al.  Adult neurogenesis in the mammalian hippocampus: Why the dentate gyrus? , 2013, Learning & memory.

[26]  S. J. Martin,et al.  The rodent hippocampus and spatial memory: from synapses to systems , 2007, Cellular and Molecular Life Sciences.

[27]  P. Luppi,et al.  Levels of Interference in Long and Short-Term Memory Differentially Modulate Non-REM and REM Sleep. , 2016, Sleep.

[28]  T. Pasternak,et al.  Working memory in primate sensory systems , 2005, Nature Reviews Neuroscience.

[29]  Hidenao Fukuyama,et al.  Tactile priming modulates the activation of the fronto-parietal circuit during tactile angle match and non-match processing: an fMRI study , 2014, Front. Hum. Neurosci..

[30]  Weizhen Xie,et al.  Affective bias in visual working memory is associated with capacity , 2017, Cognition & emotion.

[31]  W. Overman,et al.  Prolonged visual memory in macaques and man , 1980, Neuroscience.

[32]  B. Bontempi,et al.  Sites of Neocortical Reorganization Critical for Remote Spatial Memory , 2004, Science.

[33]  E. Tulving.  Multiple memory systems and consciousness. , 1987, Human neurobiology.

[34]  L. Squire,et al.  Structure and function of declarative and nondeclarative memory systems. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Alice Shaam Al Abed,et al.  Estradiol enhances retention but not organization of hippocampus-dependent memory in intact male mice , 2016, Psychoneuroendocrinology.

[36]  Rene Hen,et al.  Young and excitable: the function of new neurons in the adult mammalian brain , 2005, Current Opinion in Neurobiology.

[37]  K. Jeffery,et al.  Differential effects of spaced vs. massed training in long-term object-identity and object-location recognition memory , 2013, Behavioural Brain Research.

[38]  A. Baddeley.  The concept of working memory: A view of its current state and probable future development , 1981, Cognition.

[39]  N. Cowan,et al.  The Magical Mystery Four , 2010, Current directions in psychological science.

[40]  Michael J Kahana,et al.  Auditory Short-Term Memory Behaves Like Visual Short-Term Memory , 2007, PLoS biology.

[41]  B. Underwood,et al.  Proactive inhibition in short-term retention of single items , 1962 .

[42]  D. Olton.  Mazes, maps, and memory. , 1979, The American psychologist.

[43]  H. Eichenbaum,et al.  The Hippocampus, Memory, and Place Cells Is It Spatial Memory or a Memory Space? , 1999, Neuron.

[44]  L. Squire,et al.  Preserved learning and retention of pattern-analyzing skill in amnesia: dissociation of knowing how and knowing that. , 1980, Science.

[45]  A. Poremba,et al.  Item-nonspecific proactive interference in monkeys' auditory short-term memory , 2015, Hearing Research.

[46]  Brice A. Kuhl,et al.  The functional neuroimaging of forgetting , 2010 .

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

[48]  J. Aggleton,et al.  Qualitatively Different Hippocampal Subfield Engagement Emerges with Mastery of a Spatial Memory Task by Rats , 2008, The Journal of Neuroscience.

[49]  G. Rauchs,et al.  The relationships between memory systems and sleep stages , 2005, Journal of sleep research.

[50]  Joshua K. Hartshorne.  Visual Working Memory Capacity and Proactive Interference , 2008, PloS one.

[51]  Eric R Kandel,et al.  Bidirectional Regulation of Hippocampal Long-Term Synaptic Plasticity and Its Influence on Opposing Forms of Memory , 2010, The Journal of Neuroscience.

[52]  Clara E. Bussenius,et al.  Memory : A Contribution to Experimental Psychology , 2017 .

[53]  L. Nadel,et al.  Electroconvulsive shock and lidocaine reveal rapid consolidation of spatial working memory in the water maze. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[54]  J. P. Kincaid,et al.  Temporal gradient of release from proactive inhibition , 1970 .

[55]  N. Cowan,et al.  The role of absolute and relative amounts of time in forgetting within immediate memory: The case of tone-pitch comparisons , 1997 .

[56]  G. Miller,et al.  Plans and the structure of behavior , 1960 .

[57]  H. Pashler,et al.  Distributed practice in verbal recall tasks: A review and quantitative synthesis. , 2006, Psychological bulletin.

[58]  M. Vinken,et al.  Inhibition of Connexin43 Hemichannels Impairs Spatial Short-Term Memory without Affecting Spatial Working Memory , 2016, Front. Cell. Neurosci..

[59]  G. Tononi,et al.  Sleep function and synaptic homeostasis. , 2006, Sleep medicine reviews.

[60]  Serge Laroche,et al.  Reconsolidation of memory: A decade of debate , 2012, Progress in Neurobiology.

[61]  Jason S. Snyder,et al.  Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. , 2001, Journal of neurophysiology.

[62]  John O'Keefe,et al.  Hippocampus, theta, and spatial memory , 1993, Current Opinion in Neurobiology.

[63]  M. Johansson,et al.  Effects of facial expression on working memory. , 2016, International journal of psychology : Journal international de psychologie.

[64]  Arthur W. Joyce.  Implicit Working Memory: Implications for Assessment and Treatment , 2016, Applied neuropsychology. Child.

[65]  P. Dudchenko.  An overview of the tasks used to test working memory in rodents , 2004, Neuroscience & Biobehavioral Reviews.

[66]  Martin Eimer,et al.  Multiple foci of spatial attention in multimodal working memory , 2016, NeuroImage.

[67]  P. Roullet,et al.  Characterization of spatial memory reconsolidation , 2014, Learning & memory.

[68]  D. Spalding.  The Principles of Psychology , 1873, Nature.

[69]  E. Shimizu,et al.  Genetic enhancement of learning and memory in mice , 1999, Nature.

[70]  L. Cermak.  Decay of Interference as a Function of the Intertrial Interval in Short-Term Memory. , 1970 .

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

[72]  J. J. Donovan,et al.  A meta-analytic review of the distribution of practice effect: Now you see it, now you don't. , 1999 .

[73]  Bruce D. Gelb,et al.  The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction , 2009, Cell.

[74]  Eric R. Kandel,et al.  Transgenic Mice Lacking NMDAR-Dependent LTD Exhibit Deficits in Behavioral Flexibility , 2008, Neuron.

[75]  Hongkui Zeng,et al.  Forebrain-Specific Calcineurin Knockout Selectively Impairs Bidirectional Synaptic Plasticity and Working/Episodic-like Memory , 2001, Cell.

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

[77]  Wendy.  Now you see it....now you don , 2012 .

[78]  E. Kandel,et al.  Paradoxical influence of hippocampal neurogenesis on working memory , 2007, Proceedings of the National Academy of Sciences.

[79]  T. Carew,et al.  Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica. , 1998, Learning & memory.

[80]  Yvonne Koch.  The Psychology Of Learning And Motivation , 2016 .

[81]  Kurt Danziger,et al.  Metaphors of memory: A history of ideas about the mind , 2002 .

[82]  Paul Antoine Salin,et al.  Differential Involvement of the Dentate Gyrus in Adaptive Forgetting in the Rat , 2015, PloS one.

[83]  L. Saksida,et al.  A Functional Role for Adult Hippocampal Neurogenesis in Spatial Pattern Separation , 2009, Science.

[84]  Cindy Lustig,et al.  Escaping the recent past: Which stimulus dimensions influence proactive interference? , 2013, Memory & cognition.

[85]  Jonathan M. Golding,et al.  Adaptive forgetting in animals , 1997 .

[86]  R. Cook,et al.  Memory processing of serial lists by pigeons, monkeys, and people. , 1985, Science.