Short- and long-lasting consequences of novelty, deviance and surprise on brain and cognition

When one encounters a novel stimulus this sets off a cascade of brain responses, activating several neuromodulatory systems. As a consequence novelty has a wide range of effects on cognition; improving perception and action, increasing motivation, eliciting exploratory behavior, and promoting learning. Here, we review these benefits and how they may arise in the brain. We propose a framework that organizes novelty's effects on brain and cognition into three groups. First, novelty can transiently enhance perception. This effect is proposed to be mediated by novel stimuli activating the amygdala and enhancing early sensory processing. Second, novel stimuli can increase arousal, leading to short-lived effects on action in the first hundreds of milliseconds after presentation. We argue that these effects are related to deviance, rather than to novelty per se, and link them to activation of the locus-coeruleus norepinephrine system. Third, spatial novelty may trigger the dopaminergic mesolimbic system, promoting dopamine release in the hippocampus, having longer-lasting effects, up to tens of minutes, on motivation, reward processing, and learning and memory.

[1]  M. Merhav,et al.  Facilitation of taste memory acquisition by experiencing previous novel taste is protein-synthesis dependent. , 2008, Learning & memory.

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

[3]  E. Schröger,et al.  Attentional orienting and reorienting is indicated by human event‐related brain potentials , 1998, Neuroreport.

[4]  D. Zald The human amygdala and the emotional evaluation of sensory stimuli , 2003, Brain Research Reviews.

[5]  N. Squires,et al.  Two varieties of long-latency positive waves evoked by unpredictable auditory stimuli in man. , 1975, Electroencephalography and clinical neurophysiology.

[6]  C. Harley,et al.  Locus coeruleus activation induces perforant path-evoked population spike potentiation in the dentate gyrus of awake rat , 2004, Experimental Brain Research.

[7]  C. Harley Norepinephrine and Dopamine as Learning Signals , 2004, Neural plasticity.

[8]  B. Richmond,et al.  Relation of locus coeruleus neurons in monkeys to Pavlovian and operant behaviors. , 2009, Journal of neurophysiology.

[9]  D. Sagi,et al.  Dynamics of Memory Representations in Networks with Novelty-Facilitated Synaptic Plasticity , 2006, Neuron.

[10]  Event-related potentials during preattentional processing of color stimuli , 2008, Neuroreport.

[11]  Huafu Chen,et al.  Neural mechanism of unconscious perception of surprised facial expression , 2010, NeuroImage.

[12]  R. O’Connell,et al.  Pupil diameter covaries with BOLD activity in human locus coeruleus , 2014, Human brain mapping.

[13]  N. Lavie Perceptual load as a necessary condition for selective attention. , 1995, Journal of experimental psychology. Human perception and performance.

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

[15]  Christian F. Doeller,et al.  Movement-Related Theta Rhythm in Humans: Coordinating Self-Directed Hippocampal Learning , 2012, PLoS biology.

[16]  Neil Burgess,et al.  Human hippocampal processing of environmental novelty during spatial navigation , 2014, Hippocampus.

[17]  Ueli Rutishauser,et al.  Pupil size signals novelty and predicts later retrieval success for declarative memories of natural scenes. , 2013, Journal of vision.

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

[19]  I. Pavlov,et al.  Conditioned reflexes: An investigation of the physiological activity of the cerebral cortex. , 1929, Annals of neurosciences.

[20]  Carolyn W. Harley,et al.  A role for norepinephrine in arousal, emotion and learning?: Limbic modulation by norepinephrine and the kety hypothesis , 1987, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[21]  E Donchin,et al.  A cortical potential imaging analysis of the P300 and Novelty P3 components , 2001, Human brain mapping.

[22]  D. Manahan‐Vaughan,et al.  Beta-adrenoreceptors comprise a critical element in learning-facilitated long-term plasticity. , 2008, Cerebral cortex.

[23]  M. Gluck,et al.  Integrating incremental learning and episodic memory models of the hippocampal region. , 2005, Psychological review.

[24]  M. Meeter,et al.  Novelty Enhances Visual Perception , 2012, PloS one.

[25]  A. Üçok,et al.  Novelty P3 and P3b in first-episode schizophrenia and chronic schizophrenia , 2006, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[26]  T. Bliss,et al.  Plasticity in the human central nervous system. , 2006, Brain : a journal of neurology.

[27]  Erich Schröger,et al.  The time-course of auditory and visual distraction effects in a new crossmodal paradigm , 2010, Neuropsychologia.

[28]  P. Vuilleumier,et al.  How brains beware: neural mechanisms of emotional attention , 2005, Trends in Cognitive Sciences.

[29]  Jiang Qiu,et al.  The electrophysiological effect of working memory load on involuntary attention in an auditory–visual distraction paradigm: an ERP study , 2010, Experimental Brain Research.

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

[31]  Magnus Lindgren,et al.  Contribution of Subregions of Human Frontal Cortex to Novelty Processing , 2012, Journal of Cognitive Neuroscience.

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

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

[34]  R. O’Connell,et al.  Pupillometry and P3 index the locus coeruleus-noradrenergic arousal function in humans. , 2011, Psychophysiology.

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

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

[37]  S. Sara,et al.  Response to Novelty and its Rapid Habituation in Locus Coeruleus Neurons of the Freely Exploring Rat , 1995, The European journal of neuroscience.

[38]  C. Escera,et al.  Phasic boosting of auditory perception by visual emotion , 2013, Biological Psychology.

[39]  P. Andrés,et al.  The involuntary capture of attention by sound: novelty and postnovelty distraction in young and older adults. , 2010, Experimental psychology.

[40]  R. Simons,et al.  On the relationship of P3a and the Novelty-P3 , 2001, Biological Psychology.

[41]  Vince D. Calhoun,et al.  Genetic determinants of target and novelty-related event-related potentials in the auditory oddball response , 2009, NeuroImage.

[42]  C. Escera,et al.  Reduced novelty-P3 associated with increased behavioral distractibility in schizophrenia , 2008, Biological Psychology.

[43]  C. Harley Norepinephrine and the dentate gyrus. , 2007, Progress in brain research.

[44]  E. Phelps Emotion and cognition: insights from studies of the human amygdala. , 2006, Annual review of psychology.

[45]  Markus Ullsperger,et al.  Surprise and Error: Common Neuronal Architecture for the Processing of Errors and Novelty , 2012, The Journal of Neuroscience.

[46]  F. Parmentier,et al.  Cross-modal distraction by deviance: functional similarities between the auditory and tactile modalities. , 2012, Experimental psychology.

[47]  F. Barceló,et al.  Why are auditory novels distracting? Contrasting the roles of novelty, violation of expectation and stimulus change , 2011, Cognition.

[48]  Erich Schröger,et al.  Distraction and facilitation--two faces of the same coin? , 2012, Journal of experimental psychology. Human perception and performance.

[49]  Mark D'Esposito,et al.  Rapid Prefrontal-Hippocampal Habituation to Novel Events , 2004, The Journal of Neuroscience.

[50]  E. Schröger,et al.  The dissociation between the P3a event-related potential and behavioral distraction. , 2013, Psychophysiology.

[51]  H. Lau,et al.  Attention induces conservative subjective biases in visual perception , 2011, Nature Neuroscience.

[52]  Phillip J. Holcomb,et al.  The Influence of Stimulus Deviance on Electrophysiologic and Behavioral Responses to Novel Events , 2000, Journal of Cognitive Neuroscience.

[53]  S. L. Foote,et al.  Effects of systemic clonidine on auditory event-related potentials in squirrel monkeys , 1994, Brain Research Bulletin.

[54]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[55]  Jürgen Kayser,et al.  Event-related potentials in schizophrenia during tonal and phonetic oddball tasks: relations to diagnostic subtype, symptom features and verbal memory , 2001, Biological Psychiatry.

[56]  M. Kishiyama,et al.  The von Restorff Effect in Amnesia: The Contribution of the Hippocampal System to Novelty-Related Memory Enhancements , 2004, Journal of Cognitive Neuroscience.

[57]  R. Desimone,et al.  The representation of stimulus familiarity in anterior inferior temporal cortex. , 1993, Journal of neurophysiology.

[58]  Godfrey Pearlson,et al.  An adaptive reflexive processing model of neurocognitive function: supporting evidence from a large scale (n = 100) fMRI study of an auditory oddball task , 2005, NeuroImage.

[59]  M. Sarter,et al.  Modulators in concert for cognition: Modulator interactions in the prefrontal cortex , 2007, Progress in Neurobiology.

[60]  Mark S. Gilzenrat,et al.  Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function , 2010, Cognitive, affective & behavioral neuroscience.

[61]  W. Johnston,et al.  Novel popout: An enigma for conventional theories of attention. , 1997 .

[62]  J. Polich,et al.  P3a from Visual Stimuli: Typicality, Task, and Topography , 2004, Brain Topography.

[63]  D. Wolpert,et al.  Abnormalities in the awareness and control of action. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

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

[65]  W. Johnston,et al.  Novel popout is an attention-based phenomenon: An ERP analysis , 2000, Perception & psychophysics.

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

[67]  Sohee Park,et al.  Enhancing visual working memory encoding: The role of target novelty , 2011, Visual cognition.

[68]  J. Polich,et al.  Neuropsychology and neuropharmacology of P3a and P3b. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[69]  Mateu Sbert,et al.  An Information-Theoretic Framework for Image Complexity , 2005, CAe.

[70]  Demetrio Sierra-Mercado,et al.  Brief novelty exposure facilitates dentate gyrus LTP in aged rats , 2008, Hippocampus.

[71]  N. Lemon,et al.  Dopamine D1/D5 Receptors Gate the Acquisition of Novel Information through Hippocampal Long-Term Potentiation and Long-Term Depression , 2006, The Journal of Neuroscience.

[72]  P Andersen,et al.  Potentiation of dentate synapses initiated by exploratory learning in rats: dissociation from brain temperature, motor activity, and arousal. , 1994, Learning & memory.

[73]  R. Knight,et al.  Novelty Enhancements in Memory Are Dependent on Lateral Prefrontal Cortex , 2009, The Journal of Neuroscience.

[74]  S. L. Foote,et al.  Locus coeruleus neuronal activity in awake monkeys: relationship to auditory P300-like potentials and spontaneous EEG , 2004, Experimental Brain Research.

[75]  M. Bradley Natural selective attention: orienting and emotion. , 2009, Psychophysiology.

[76]  Godfrey D Pearlson,et al.  An FMRI auditory oddball study of combined-subtype attention deficit hyperactivity disorder. , 2007, The American journal of psychiatry.

[77]  M. Meeter,et al.  Happier, faster: Developmental changes in the effects of mood and novelty on responses , 2016, Quarterly journal of experimental psychology.

[78]  M Meeter,et al.  Mode shifting between storage and recall based on novelty detection in oscillating hippocampal circuits , 2004, Hippocampus.

[79]  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.

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

[81]  Therese van Amelsvoort,et al.  The Detection of Novelty Relies on Dopaminergic Signaling: Evidence from Apomorphine's Impact on the Novelty N2 , 2013, PloS one.

[82]  Peter Dayan,et al.  Dopamine: generalization and bonuses , 2002, Neural Networks.

[83]  Sander Nieuwenhuis,et al.  Pupil Diameter Predicts Changes in the Exploration–Exploitation Trade-off: Evidence for the Adaptive Gain Theory , 2011, Journal of Cognitive Neuroscience.

[84]  R. Näätänen Attention and brain function , 1992 .

[85]  P. Hagoort,et al.  The suppression of repetition enhancement: A review of fMRI studies , 2013, Neuropsychologia.

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

[87]  H. Nittono,et al.  Unexpected action effects elicit deviance-related brain potentials and cause behavioral delay. , 2010, Psychophysiology.

[88]  C. Harley,et al.  Novelty‐elicited, Noradrenaline‐dependent Enhancement of Excitability in the Dentate Gyrus , 1997, The European journal of neuroscience.

[89]  J Altarriba,et al.  Novel popout without novelty , 1998, Memory & cognition.

[90]  Daniel B Mark,et al.  Facets of Openness Predict Mortality in Patients With Cardiac Disease , 2007, Psychosomatic medicine.

[91]  Bradford C. Dickerson,et al.  Novelty as a dimension in the affective brain , 2010, NeuroImage.

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

[93]  T. Jay Dopamine: a potential substrate for synaptic plasticity and memory mechanisms , 2003, Progress in Neurobiology.

[94]  Jennifer Urbano Blackford,et al.  A unique role for the human amygdala in novelty detection , 2010, NeuroImage.

[95]  Nico Bunzeck,et al.  Reward Motivation Accelerates the Onset of Neural Novelty Signals in Humans to 85 Milliseconds , 2009, Current Biology.

[96]  Daniel Kahneman,et al.  Remarks on attention control , 1970 .

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

[98]  E. Clark,et al.  Is perceptual salience needed in explanations of the isolation effect? , 2000, Journal of experimental psychology. Learning, memory, and cognition.

[99]  Jutta S. Mayer,et al.  Failure to benefit from target novelty during encoding contributes to working memory deficits in schizophrenia , 2014, Cognitive neuropsychiatry.

[100]  M. Guitart-Masip,et al.  NOvelty-related Motivation of Anticipation and exploration by Dopamine (NOMAD): Implications for healthy aging , 2010, Neuroscience & Biobehavioral Reviews.

[101]  Jerome Kagan,et al.  Differential amygdalar response to novel versus newly familiar neutral faces: a functional MRI probe developed for studying inhibited temperament , 2003, Biological Psychiatry.

[102]  M. Hasselmo,et al.  Differences in time course of ACh and GABA modulation of excitatory synaptic potentials in slices of rat hippocampus. , 2001, Journal of neurophysiology.

[103]  Erich Schröger,et al.  Auditory distraction: event-related potential and behavioral indices , 2000, Clinical Neurophysiology.

[104]  J. Pineda,et al.  Effects of locus coeruleus lesions on auditory, long-latency, event- related potentials in monkey , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[105]  M. Hasselmo The role of acetylcholine in learning and memory , 2006, Current Opinion in Neurobiology.

[106]  M. Hasselmo,et al.  Encoding and retrieval of episodic memories: Role of cholinergic and GABAergic modulation in the hippocampus , 1998, Hippocampus.

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

[108]  E. Donchin Presidential address, 1980. Surprise!...Surprise? , 1981, Psychophysiology.

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

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

[111]  István Czigler,et al.  Memory-based detection of task-irrelevant visual changes. , 2002, Psychophysiology.

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

[113]  S. Sara The locus coeruleus and noradrenergic modulation of cognition , 2009, Nature Reviews Neuroscience.

[114]  M. Meeter,et al.  Facilitation of responses by task-irrelevant complex deviant stimuli. , 2014, Acta psychologica.

[115]  E. Donchin,et al.  Localization of the event-related potential novelty response as defined by principal components analysis. , 2003, Brain research. Cognitive brain research.

[116]  J. Sergeant,et al.  When distraction is not distracting: A behavioral and ERP study on distraction in ADHD , 2007, Clinical Neurophysiology.

[117]  D. Linden,et al.  Attention capture by novel sounds: Distraction versus facilitation , 2010 .

[118]  E. N. Sokolov The orienting response, and future directions of its development , 1990, The Pavlovian journal of biological science.

[119]  L. Bianchi,et al.  Effects of novelty and habituation on acetylcholine, GABA, and glutamate release from the frontal cortex and hippocampus of freely moving rats , 2001, Neuroscience.

[120]  Markus Ullsperger,et al.  Lesions to the prefrontal performance-monitoring network disrupt neural processing and adaptive behaviors after both errors and novelty , 2014, Cortex.

[121]  E. Schröger,et al.  A comparison of auditory and visual distraction effects: behavioral and event-related indices. , 2001, Brain research. Cognitive brain research.

[122]  J. Frey,et al.  Cholinergic afferents to the locus coeruleus and noradrenergic afferents to the medial septum mediate LTP-reinforcement in the dentate gyrus by stimulation of the amygdala , 2007, Neurobiology of Learning and Memory.

[123]  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.

[124]  W. K. Cullen,et al.  Dopamine-dependent facilitation of LTP induction in hippocampal CA1 by exposure to spatial novelty , 2003, Nature Neuroscience.

[125]  C. Montigny,et al.  The serotonergic and noradrenergic systems of the hippocampus: their interactions and the effects of antidepressant treatments , 1997, Brain Research Reviews.

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

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

[128]  A. Anderson,et al.  Lesions of the human amygdala impair enhanced perception of emotionally salient events , 2001, Nature.

[129]  B. Jacobs,et al.  Single unit activity of locus coeruleus neurons in the freely moving cat I. During naturalistic behaviors and in response to simple and complex stimuli , 1986, Brain Research.

[130]  M. Meeter,et al.  Electrophysiological analysis of the role of novelty in the von Restorff effect , 2013, Brain and behavior.

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

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

[133]  J. Panksepp Affective Neuroscience: The Foundations of Human and Animal Emotions , 1998 .

[134]  R. Morris,et al.  From Rapid Place Learning to Behavioral Performance: A Key Role for the Intermediate Hippocampus , 2009, PLoS biology.

[135]  D. Kahneman,et al.  Attention and Effort , 1973 .

[136]  Rolf Verleger,et al.  P3b: Towards some decision about memory , 2008, Clinical Neurophysiology.

[137]  Thomas Straube,et al.  Requirement of β‐adrenergic receptor activation and protein synthesis for LTP‐reinforcement by novelty in rat dentate gyrus , 2003 .

[138]  Alison Adcock,et al.  Enriched encoding: reward motivation organizes cortical networks for hippocampal detection of unexpected events. , 2014, Cerebral cortex.

[139]  Stefan Berti,et al.  Object switching within working memory is reflected in the human event-related brain potential , 2008, Neuroscience Letters.

[140]  James G. Heys,et al.  Possible role of acetylcholine in regulating spatial novelty effects on theta rhythm and grid cells , 2012, Front. Neural Circuits.

[141]  S. R. Schmidt Encoding and retrieval processes in the memory for conceptually distinctive events. , 1985, Journal of experimental psychology. Learning, memory, and cognition.

[142]  Carles Escera,et al.  When Loading Working Memory Reduces Distraction: Behavioral and Electrophysiological Evidence from an Auditory-Visual Distraction Paradigm , 2008, Journal of Cognitive Neuroscience.

[143]  James L McGaugh,et al.  Emotional arousal and enhanced amygdala activity: new evidence for the old perseveration-consolidation hypothesis. , 2005, Learning & memory.

[144]  Jeffrey C. Cooper,et al.  The Lure of the Unknown , 2006, Neuron.

[145]  F. Waszak,et al.  Effect anticipation modulates deviance processing in the brain , 2007, Brain Research.

[146]  N. Lavie,et al.  Harnessing the wandering mind: The role of perceptual load , 2009, Cognition.

[147]  R. Nicoll,et al.  Actions of noradrenaline recorded intracellularly in rat hippocampal CA1 pyramidal neurones, in vitro. , 1986, The Journal of physiology.

[148]  R. Knight Contribution of human hippocampal region to novelty detection , 1996, Nature.

[149]  E. Donchin,et al.  A componential analysis of the ERP elicited by novel events using a dense electrode array. , 1999, Psychophysiology.

[150]  Erich Schröger,et al.  Distraction effects in vision: behavioral and event-related potential indices , 2004, Neuroreport.

[151]  J. Behr,et al.  Activation of dopamine D1/D5 receptors facilitates the induction of presynaptic long‐term potentiation at hippocampal output synapses , 2010, The European journal of neuroscience.

[152]  S. Sara,et al.  Locus coeruleus-evoked responses in behaving rats: A clue to the role of noradrenaline in memory , 1994, Brain Research Bulletin.

[153]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[154]  C. Escera,et al.  Electrical responses reveal the temporal dynamics of brain events during involuntary attention switching , 2001, The European journal of neuroscience.

[155]  D. Carmelli,et al.  Curiosity and mortality in aging adults: a 5-year follow-up of the Western Collaborative Group Study. , 1996, Psychology and aging.

[156]  R. Dolan,et al.  Contextual Novelty Changes Reward Representations in the Striatum , 2010, The Journal of Neuroscience.

[157]  Jessica K. Ljungberg,et al.  Behavioral distraction by auditory novelty is not only about novelty: The role of the distracter’s informational value , 2010, Cognition.

[158]  E. Hazlett,et al.  The relationship between skin conductance orienting and the allocation of processing resources. , 1991, Psychophysiology.

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

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

[161]  R. Klein,et al.  Assessing the evidence for novel popout. , 1996 .

[162]  C. Bradshaw,et al.  Comparison of the effects of clonidine and yohimbine on pupillary diameter at different illumination levels. , 2000, British journal of clinical pharmacology.

[163]  E. Düzel,et al.  The novelty exploration bonus and its attentional modulation , 2009, Neuropsychologia.

[164]  M. Meeter,et al.  Novelty detection is enhanced when attention is otherwise engaged: an event-related potential study , 2014, Experimental Brain Research.

[165]  Ruth M. Krebs,et al.  Novelty increases the mesolimbic functional connectivity of the substantia nigra/ventral tegmental area (SN/VTA) during reward anticipation: Evidence from high-resolution fMRI , 2011, NeuroImage.

[166]  N. Bunzeck,et al.  Dopamine Controls the Neural Dynamics of Memory Signals and Retrieval Accuracy , 2013, Neuropsychopharmacology.

[167]  R. Knight Decreased response to novel stimuli after prefrontal lesions in man. , 1984, Electroencephalography and clinical neurophysiology.

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

[169]  M. Hasselmo Neuromodulation: acetylcholine and memory consolidation , 1999, Trends in Cognitive Sciences.

[170]  Rafal Bogacz,et al.  Comparison of computational models of familiarity discrimination in the perirhinal cortex , 2003, Hippocampus.

[171]  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 .

[172]  Karl J. Friston,et al.  A neuromodulatory role for the human amygdala in processing emotional facial expressions. , 1998, Brain : a journal of neurology.

[173]  M. W. Brown,et al.  Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe , 1998, Neuropharmacology.

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

[175]  M. Recce,et al.  Memory for places: A navigational model in support of Marr's theory of hippocampal function , 1996, Hippocampus.

[176]  Erich Schröger,et al.  Visual distraction: a behavioral and event-related brain potential study in humans , 2006, Neuroreport.

[177]  J. Polich,et al.  P300 amplitude is determined by target-to-target interval. , 2002, Psychophysiology.

[178]  E. Schröger,et al.  The development of involuntary and voluntary attention from childhood to adulthood: A combined behavioral and event-related potential study , 2006, Clinical Neurophysiology.

[179]  J. Polich,et al.  Normative Variation of P3a and P3b from a Large Sample , 2007 .

[180]  T. Knapen,et al.  Decision-related pupil dilation reflects upcoming choice and individual bias , 2014, Proceedings of the National Academy of Sciences.

[181]  Jessica K Ljungberg,et al.  A behavioral study of distraction by vibrotactile novelty. , 2011, Journal of experimental psychology. Human perception and performance.

[182]  E. Schröger,et al.  Bottom-up influences on working memory: behavioral and electrophysiological distraction varies with distractor strength. , 2004, Experimental psychology.

[183]  Gary Aston-Jones,et al.  Responses of primate locus coeruleus neurons to simple and complex sensory stimuli , 1988, Brain Research Bulletin.

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

[185]  Denise Manahan-Vaughan,et al.  The hippocampal CA1 region and dentate gyrus differentiate between environmental and spatial feature encoding through long-term depression. , 2008, Cerebral cortex.

[186]  Nico Bunzeck,et al.  Dopamine modulates processing speed in the human mesolimbic system , 2013, NeuroImage.

[187]  I. Winkler,et al.  Involuntary Attention and Distractibility as Evaluated with Event-Related Brain Potentials , 2000, Audiology and Neurotology.

[188]  Judith M Ford,et al.  Anticipating the future: automatic prediction failures in schizophrenia. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[189]  Y. D. van der Werf,et al.  Novelty processing and memory formation in Parkinson׳s disease , 2014, Neuropsychologia.

[190]  F. Craik,et al.  Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[191]  R. Henson,et al.  Memory signals are temporally dissociated within and across human hippocampus and perirhinal cortex , 2012, Nature Neuroscience.

[192]  S. Sajikumar,et al.  Late-associativity, synaptic tagging, and the role of dopamine during LTP and LTD , 2004, Neurobiology of Learning and Memory.

[193]  G. M. Reicher,et al.  Familiarity of background characters in visual scanning. , 1976, Journal of experimental psychology. Human perception and performance.

[194]  Stefan Berti,et al.  Examining task-dependencies of different attentional processes as reflected in the P3a and reorienting negativity components of the human event-related brain potential , 2006, Neuroscience Letters.

[195]  D. Bruce,et al.  Tests of an Organizational Hypothesis of Isolation Effects in Free Recall. , 1976 .

[196]  Stephen J. Boies,et al.  Components of attention. , 1971 .

[197]  M. Hasselmo Neuromodulation and cortical function: modeling the physiological basis of behavior , 1995, Behavioural Brain Research.

[198]  Christopher I. Wright,et al.  Novelty responses and differential effects of order in the amygdala, substantia innominata, and inferior temporal cortex , 2003, NeuroImage.

[199]  E. Donchin,et al.  Spatiotemporal analysis of the late ERP responses to deviant stimuli. , 2001, Psychophysiology.

[200]  Helen M. Morgan,et al.  On the functional significance of Novelty-P3: Facilitation by unexpected novel sounds , 2010, Biological Psychology.

[201]  Nico Bunzeck,et al.  Contextual interaction between novelty and reward processing within the mesolimbic system , 2011, Human brain mapping.

[202]  F. Parmentier,et al.  Distraction by auditory novelty. The course and aftermath of novelty and semantic effects. , 2011, Experimental psychology.

[203]  Colin Hawco,et al.  Overlapping patterns of neural activity for different forms of novelty in fMRI , 2014, Front. Hum. Neurosci..

[204]  Elizabeth A Buffalo,et al.  Recognition memory signals in the macaque hippocampus , 2009, Proceedings of the National Academy of Sciences.

[205]  Jonathan D. Cohen,et al.  Adaptive gain and the role of the locus coeruleus–norepinephrine system in optimal performance , 2005, The Journal of comparative neurology.