Novelty Manipulations, Memory Performance, and Predictive Coding: the Role of Unexpectedness

Novelty is central to the study of memory, but the wide range of experimental manipulations aimed to reveal its effects on learning produced inconsistent results. The novelty/encoding hypothesis suggests that novel information undergoes enhanced encoding and thus leads to benefits in memory, especially in recognition performance; however, recent studies cast doubts on this assumption. On the other hand, data from animal studies provided evidence on the robust effects of novelty manipulations on the neurophysiological correlates of memory processes. Conceptualizations and operationalizations of novelty are remarkably variable and were categorized into different subtypes, such as stimulus, context, associative or spatial novelty. Here, we summarize previous findings about the effects of novelty on memory and suggest that predictive coding theories provide a framework that could shed light on the differential influence of novelty manipulations on memory performance. In line with predictive coding theories, we emphasize the role of unexpectedness as a crucial property mediating the behavioral and neural effects of novelty manipulations.

[1]  Daniela Montaldi,et al.  How do memory systems detect and respond to novelty? , 2018, Neuroscience Letters.

[2]  E. Tulving,et al.  Novelty encoding networks in the human brain: positron emission tomography data. , 1994, Neuroreport.

[3]  M M Mesulam,et al.  An electrophysiological index of stimulus unfamiliarity. , 2000, Psychophysiology.

[4]  D. Knill,et al.  The Bayesian brain: the role of uncertainty in neural coding and computation , 2004, Trends in Neurosciences.

[5]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[6]  C. Nelson,et al.  Age-related changes in the electrophysiological response to visual stimulus novelty: a topographical approach. , 1996, Electroencephalography and clinical neurophysiology.

[7]  Mareike Grotheer,et al.  The relationship between stimulus repetitions and fulfilled expectations , 2015, Neuropsychologia.

[8]  T Seidenbecher,et al.  Task‐relevant late positive component in rats: Is it related to hippocampal theta rhythm? , 1996, Hippocampus.

[9]  Jim M. Monti,et al.  Neural repetition suppression reflects fulfilled perceptual expectations , 2008, Nature Neuroscience.

[10]  R. Vogels,et al.  Repetition Probability Does Not Affect fMRI Repetition Suppression for Objects , 2013, The Journal of Neuroscience.

[11]  F. Craik,et al.  Novelty and familiarity activations in PET studies of memory encoding and retrieval. , 1996, Cerebral cortex.

[12]  A. Grace,et al.  Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission , 2003, Nature Neuroscience.

[13]  Yadin Dudai,et al.  Knowledge acquisition is governed by striatal prediction errors , 2018, Nature Communications.

[14]  M. Penttonen,et al.  Behavioral and hippocampal evoked responses in an auditory oddball situation when an unconditioned stimulus is paired with deviant tones in the cat: experiment II. , 1995, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  E. Kandel,et al.  Dopamine release from the locus coeruleus to the dorsal hippocampus promotes spatial learning and memory , 2016, Proceedings of the National Academy of Sciences.

[16]  Guy M. Goodwin,et al.  The role of the anterior cingulate cortex in the counting Stroop task , 2004, Experimental Brain Research.

[17]  D. Kumaran,et al.  Match–Mismatch Processes Underlie Human Hippocampal Responses to Associative Novelty , 2007, The Journal of Neuroscience.

[18]  R. Habib,et al.  Activation of midbrain structures by associative novelty and the formation of explicit memory in humans. , 2004, Learning & memory.

[19]  B. Kopp,et al.  Prior probabilities modulate cortical surprise responses: A study of event-related potentials , 2016, Brain and Cognition.

[20]  Hans-Jochen Heinze,et al.  Human Hippocampal and Parahippocampal Activity during Visual Associative Recognition Memory for Spatial and Nonspatial Stimulus Configurations , 2003, The Journal of Neuroscience.

[21]  Clay B. Holroyd,et al.  A Novel Neural Prediction Error Found in Anterior Cingulate Cortex Ensembles , 2017, Neuron.

[22]  Wolfram Schultz,et al.  Dopamine reward prediction-error signalling: a two-component response , 2016, Nature Reviews Neuroscience.

[23]  D. Berlyne Conflict, arousal, and curiosity , 2014 .

[24]  D. Bavelier,et al.  Influence of reward motivation on human declarative memory , 2016, Neuroscience & Biobehavioral Reviews.

[25]  W. Schultz,et al.  Responses of monkey dopamine neurons during learning of behavioral reactions. , 1992, Journal of neurophysiology.

[26]  E. Donchin,et al.  “P300” and memory: Individual differences in the von Restorff effect , 1984, Cognitive Psychology.

[27]  Phillip J. Holcomb,et al.  To Ignore or Explore: Top-Down Modulation of Novelty Processing , 2008, J. Cogn. Neurosci..

[28]  N. Daw,et al.  Striatal Activity Underlies Novelty-Based Choice in Humans , 2008, Neuron.

[29]  Yves De Koninck,et al.  Normal and abnormal coding of somatosensory stimuli causing pain , 2014, Nature Neuroscience.

[30]  A. Todorović,et al.  Repetition Suppression and Expectation Suppression Are Dissociable in Time in Early Auditory Evoked Fields , 2012, The Journal of Neuroscience.

[31]  Hans-Jochen Heinze,et al.  Novel Scenes Improve Recollection and Recall of Words , 2008, Journal of Cognitive Neuroscience.

[32]  A. Clark Whatever next? Predictive brains, situated agents, and the future of cognitive science. , 2013, The Behavioral and brain sciences.

[33]  E. Düzel,et al.  Personality Traits Are Differentially Associated with Patterns of Reward and Novelty Processing in the Human Substantia Nigra/Ventral Tegmental Area , 2009, Biological Psychiatry.

[34]  H. V. Restorff Über die Wirkung von Bereichsbildungen im Spurenfeld , 1933 .

[35]  H. Heinze,et al.  The Dopaminergic Midbrain Participates in Human Episodic Memory Formation: Evidence from Genetic Imaging , 2006, The Journal of Neuroscience.

[36]  Mark G. Packard,et al.  Anterograde and retrograde tracing of projections from the ventral tegmental area to the hippocampal formation in the rat , 1994, Brain Research Bulletin.

[37]  Lars Nyberg,et al.  Any novelty in hippocampal formation and memory? , 2005, Current opinion in neurology.

[38]  Y. Dudai,et al.  Neuroscience and Biobehavioral Reviews Peri-encoding Predictors of Memory Encoding and Consolidation , 2022 .

[39]  F. D. Lange,et al.  How Do Expectations Shape Perception? , 2018, Trends in Cognitive Sciences.

[40]  Carsten Nicolas Boehler,et al.  Neural correlates of exemplar novelty processing under different spatial attention conditions , 2009, Human brain mapping.

[41]  S. Nieuwenhuis,et al.  The anatomical and functional relationship between the P3 and autonomic components of the orienting response. , 2011, Psychophysiology.

[42]  E. Courchesne,et al.  Stimulus novelty, task relevance and the visual evoked potential in man. , 1975, Electroencephalography and clinical neurophysiology.

[43]  Walter Ritter,et al.  The N2 component elicited by stimulus matches and multiple targets , 1988, Biological Psychology.

[44]  J. Frey,et al.  Bidirectional modulation of long-term potentiation by novelty-exploration in rat dentate gyrus , 2003, Neuroscience Letters.

[45]  Emrah Duzel,et al.  A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP , 2011, Trends in Neurosciences.

[46]  A. Grace,et al.  Glutamatergic Afferents from the Hippocampus to the Nucleus Accumbens Regulate Activity of Ventral Tegmental Area Dopamine Neurons , 2001, The Journal of Neuroscience.

[47]  Richard N Henson,et al.  Predictive, interactive multiple memory systems , 2010, Hippocampus.

[48]  Rufin Vogels,et al.  Stimulus repetition probability does not affect repetition suppression in macaque inferior temporal cortex. , 2011, Cerebral cortex.

[49]  J. Schomaker Unexplored territory: Beneficial effects of novelty on memory , 2019, Neurobiology of Learning and Memory.

[50]  D. Friedman,et al.  The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty , 2001, Neuroscience & Biobehavioral Reviews.

[51]  M. W. Brown,et al.  Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: a c-fos expression study , 2004, Neuroscience.

[52]  C. Stern,et al.  Prefrontal–Temporal Circuitry for Episodic Encoding and Subsequent Memory , 2000, The Journal of Neuroscience.

[53]  Lars-Göran Nilsson,et al.  The novelty effect: support for the Novelty-Encoding Hypothesis. , 2005, Scandinavian journal of psychology.

[54]  Berrin Maraşligil,et al.  İnsanlarda Yenilik N2 Yanıtı Hedef Uyaranların Zamansal Sınıflamasını Yansıtır , 2011 .

[55]  Ian C. Ballard,et al.  Hippocampal networks habituate as novelty accumulates. , 2013, Learning & memory.

[56]  R. Wise,et al.  Novelty‐evoked elevations of nucleus accumbens dopamine: dependence on impulse flow from the ventral subiculum and glutamatergic neurotransmission in the ventral tegmental area , 2001, The European journal of neuroscience.

[57]  A. Buss,et al.  Personality Traits , 1973 .

[58]  S. Tonegawa,et al.  Locus coeruleus input to hippocampal CA3 drives single-trial learning of a novel context , 2017, Proceedings of the National Academy of Sciences.

[59]  Anat Maril,et al.  Distinctiveness Benefits Novelty (and Not Familiarity), but Only Up to a Limit: The Prior Knowledge Perspective , 2018, Cogn. Sci..

[60]  D. Kumaran,et al.  An Unexpected Sequence of Events: Mismatch Detection in the Human Hippocampus , 2006, PLoS biology.

[61]  G. Tononi,et al.  Dreaming and the brain: from phenomenology to neurophysiology , 2010, Trends in Cognitive Sciences.

[62]  G. Rainer,et al.  Cognitive neuroscience: Neural mechanisms for detecting and remembering novel events , 2003, Nature Reviews Neuroscience.

[63]  Floris P. de Lange,et al.  How Prediction Errors Shape Perception, Attention, and Motivation , 2012, Front. Psychology.

[64]  M. Meeter,et al.  Short- and long-lasting consequences of novelty, deviance and surprise on brain and cognition , 2015, Neuroscience & Biobehavioral Reviews.

[65]  E. Tulving,et al.  Novelty assessment in the brain and long-term memory encoding , 1995, Psychonomic bulletin & review.

[66]  Kerstin Preuschoff,et al.  Balancing New against Old Information: The Role of Puzzlement Surprise in Learning , 2018, Neural Computation.

[67]  Phillip J Holcomb,et al.  Surprise? Early visual novelty processing is not modulated by attention. , 2011, Psychophysiology.

[68]  L. Geraci,et al.  Please Scroll down for Article the Quarterly Journal of Experimental Psychology Distinctive Items Are Salient during Encoding: Delayed Judgements of Learning Predict the Isolation Effect , 2022 .

[69]  L. Balázs,et al.  Stimulus complexity effects on the event-related potentials to task-irrelevant stimuli , 2013, Biological Psychology.

[70]  A. Barto,et al.  Novelty or Surprise? , 2013, Front. Psychol..

[71]  J. Lisman,et al.  The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory , 2005, Neuron.

[72]  R. Henson,et al.  Does prediction error drive one-shot declarative learning? , 2017, Journal of memory and language.

[73]  Jonathan R. Folstein,et al.  Influence of cognitive control and mismatch on the N2 component of the ERP: a review. , 2007, Psychophysiology.

[74]  M. Bradley,et al.  Massed and distributed repetition of natural scenes: Brain potentials and oscillatory activity. , 2015, Psychophysiology.

[75]  M. Meeter,et al.  Expecting the unexpected: the effects of deviance on novelty processing. , 2014, Behavioral neuroscience.

[76]  Mareike Grotheer,et al.  Repetition Probability Effects Depend on Prior Experiences , 2014, The Journal of Neuroscience.

[77]  Karl J. Friston,et al.  Waking and dreaming consciousness: Neurobiological and functional considerations , 2012, Progress in Neurobiology.

[78]  Carson C. Chow,et al.  Repetition priming and repetition suppression: A case for enhanced efficiency through neural synchronization , 2012, Cognitive neuroscience.

[79]  M. Meeter,et al.  Predicting the unknown: Novelty processing depends on expectations , 2018, Brain Research.

[80]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[81]  N. Bunzeck,et al.  Absolute Coding of Stimulus Novelty in the Human Substantia Nigra/VTA , 2006, Neuron.

[82]  F. L. Jones,et al.  Novel Environments Enhance the Induction and Maintenance of Long-Term Potentiation in the Dentate Gyrus , 2004, The Journal of Neuroscience.

[83]  J. O’Keefe,et al.  Environmental novelty is signaled by reduction of the hippocampal theta frequency , 2008, Hippocampus.

[84]  Martijn Meeter,et al.  Exploring a novel environment improves motivation and promotes recall of words , 2014, Front. Psychol..

[85]  Karl J. Friston,et al.  Repetition suppression and its contextual determinants in predictive coding , 2016, Cortex.

[86]  R. Henson,et al.  How schema and novelty augment memory formation , 2012, Trends in Neurosciences.

[87]  Timothy E. J. Behrens,et al.  Dissociable effects of surprise and model update in parietal and anterior cingulate cortex , 2013, Proceedings of the National Academy of Sciences.

[88]  D. Shohamy,et al.  Dopamine and adaptive memory , 2010, Trends in Cognitive Sciences.

[89]  P. Holland,et al.  Role of Substantia Nigra–Amygdala Connections in Surprise-Induced Enhancement of Attention , 2006, The Journal of Neuroscience.

[90]  K. Grill-Spector,et al.  Repetition and the brain: neural models of stimulus-specific effects , 2006, Trends in Cognitive Sciences.

[91]  Karl J. Friston,et al.  A theory of cortical responses , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[92]  A. Yonelinas,et al.  Distinctiveness in Recognition and Free Recall: The Role of Recollection in the Rejection of the Familiar☆☆☆★ , 1998 .

[93]  C. Verney,et al.  Mesolimbic dopaminergic neurons innervating the hippocampal formation in the rat: a combined retrograde tracing and immunohistochemical study , 1994, Brain Research.

[94]  William H. Alexander,et al.  The Role of the Anterior Cingulate Cortex in Prediction Error and Signaling Surprise , 2019, Top. Cogn. Sci..

[95]  J. Frey,et al.  Reinforcement of rat hippocampal LTP by holeboard training. , 2005, Learning & memory.

[96]  G. Stefanics,et al.  Visual mismatch negativity: a predictive coding view , 2014, Front. Hum. Neurosci..

[97]  Raymond J. Dolan,et al.  Anticipation of novelty recruits reward system and hippocampus while promoting recollection , 2007, NeuroImage.

[98]  Gernot Horstmann,et al.  The Cognitive-Evolutionary Model of Surprise: A Review of the Evidence , 2019, Top. Cogn. Sci..

[99]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[100]  M Moscovitch,et al.  Revisiting the novelty effect: when familiarity, not novelty, enhances memory. , 2010, Journal of experimental psychology. Learning, memory, and cognition.

[101]  E. N. Sokolov Higher nervous functions; the orienting reflex. , 1963, Annual review of physiology.

[102]  R. Dolan,et al.  Knowing how much you don't know: a neural organization of uncertainty estimates , 2012, Nature Reviews Neuroscience.

[103]  G. Kovács,et al.  Can predictive coding explain repetition suppression? , 2016, Cortex.

[104]  Hans-Jochen Heinze,et al.  Mesolimbic novelty processing in older adults. , 2007, Cerebral cortex.

[105]  Ravi S. Menon,et al.  Novelty responses to relational and non‐relational information in the hippocampus and the parahippocampal region: A comparison based on event‐related fMRI , 2005, Hippocampus.

[106]  István Czigler,et al.  Age-related effects of novel visual stimuli in a letter-matching task: an event-related potential study , 2005, Biological Psychology.