The Influence of Stimulus Deviance on Electrophysiologic and Behavioral Responses to Novel Events

This study investigated the role of stimulus deviance in determining electrophysiologic and behavioral responses to novelty. Stimulus deviance was defined in terms of differences either from the immediately preceding context or from long-term experience. Subjects participated in a visual event-related potential (ERP) experiment, in which they controlled the duration of stimulus viewing with a button press, which served as a measure of exploratory behavior. Each of the three experimental conditions included a frequent repetitive background stimulus and infrequent stimuli that deviated from the background stimulus. In one condition, both background and deviant stimuli were simple, easily recognizable geometric figures. In another condition, both background and deviant stimuli were unusual/unfamiliar figures, and in a third condition, the background stimulus was a highly unusual figure, and the deviant stimuli were simple, geometric shapes. Deviant stimuli elicited larger N2-P3 amplitudes and longer viewing durations than the repetitive background stimulus, even when the deviant stimuli were simple, familiar shapes and the background stimulus was a highly unusual figure. Compared to simple, familiar deviant stimuli, unusual deviant stimuli elicited larger N2-P3 amplitudes and longer viewing times. Within subjects, the deviant stimuli that evoked the largest N2-P3 responses also elicited the longest viewing durations. We conclude that deviance from both immediate context and long-term prior experience contribute to the response to novelty, with the combination generating the largest N2-P3 amplitude and the most sustained attention. The amplitude of the N2-P3 may reflect how much uncertainty is evoked by a novel visual stimulus and signal the need for further exploration and cognitive processing.

[1]  S M Kosslyn,et al.  Identifying objects seen from different viewpoints. A PET investigation. , 1994, Brain : a journal of neurology.

[2]  J Metcalfe Novelty monitoring, metacognition, and control in a composite holographic associative recall model: implications for Korsakoff amnesia. , 1993, Psychological review.

[3]  M. Mesulam,et al.  The central role of the prefrontal cortex in directing attention to novel events. , 2000, Brain : a journal of neurology.

[4]  W. Ritter,et al.  Orienting and habituation to auditory stimuli: a study of short term changes in average evoked responses. , 1968, Electroencephalography and clinical neurophysiology.

[5]  W. Roth,et al.  Auditory evoked responses to unpredictable stimuli. , 1973, Psychophysiology.

[6]  V. Mountcastle,et al.  Higher functions of the brain , 1987 .

[7]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. III. Frontal cortex. , 1995, Electroencephalography and clinical neurophysiology.

[8]  S. Hillyard,et al.  Long-latency evoked potentials to irrelevant, deviant stimuli. , 1976, Behavioral biology.

[9]  M. Mesulam,et al.  Diminished curiosity in patients with probable Alzheimer's disease as measured by exploratory eye movements , 1992, Neurology.

[10]  N. Humphrey ‘Interest’ and ‘Pleasure’: Two Determinants of a Monkey's Visual Preferences , 1972, Perception.

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

[12]  E Courchesne,et al.  Changes in P3 waves with event repetition: long-term effects on scalp distribution and amplitude. , 1978, Electroencephalography and clinical neurophysiology.

[13]  S. Geisser,et al.  On methods in the analysis of profile data , 1959 .

[14]  G. F. Tremblay,et al.  The Prefrontal Cortex , 1989, Neurology.

[15]  T W Picton,et al.  The P300 Wave of the Human Event‐Related Potential , 1992, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[16]  Judith F. Kroll,et al.  Recognizing words, pictures, and concepts: A comparison of lexical, object, and reality decisions , 1984 .

[17]  N. Mackworth,et al.  The gaze selects informative details within pictures , 1967 .

[18]  Ray Johnson For Distinguished Early Career Contribution to Psychophysiology: Award Address, 1985 , 1986 .

[19]  J. Polich,et al.  P3a, perceptual distinctiveness, and stimulus modality. , 1998, Brain research. Cognitive brain research.

[20]  N. Mackworth,et al.  Cognitive determinants of fixation location during picture viewing. , 1978, Journal of experimental psychology. Human perception and performance.

[21]  D. Noton,et al.  Eye movements and visual perception. , 1971, Scientific American.

[22]  Steven A. Hillyard,et al.  The effect of stimulus deviation on P3 waves to easily recognized stimuli , 1978, Neuropsychologia.

[23]  M. Mesulam,et al.  The impact of aging on curiosity as measured by exploratory eye movements. , 1994, Archives of neurology.

[24]  R. Almond The therapeutic community. , 1971, Scientific American.

[25]  H. Spinnler The prefrontal cortex, Anatomy, physiology, and neuropsychology of the frontal lobe, J.M. Fuster. Raven Press, New York (1980), IX-222 pages , 1981 .

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

[27]  Risto Näätänen,et al.  5 The Orienting Reflex and the N2 Deflection of the Event-Related Potential (ERP) , 1983 .

[28]  E. Donchin,et al.  Is the P300 component a manifestation of context updating? , 1988, Behavioral and Brain Sciences.

[29]  R. Johnson A triarchic model of P300 amplitude. , 1986, Psychophysiology.

[30]  T W Picton,et al.  N2 and automatic versus controlled processes. , 1986, Electroencephalography and clinical neurophysiology. Supplement.

[31]  J. Kounios,et al.  Concreteness effects in semantic processing: ERP evidence supporting dual-coding theory. , 1994, Journal of experimental psychology. Learning, memory, and cognition.

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

[33]  M. Posner Chronometric explorations of mind : the third Paul M. Fitts lectures, delivered at the University of Michigan, September 1976 , 1978 .

[34]  C. C. Wood,et al.  Scalp distributions of event-related potentials: an ambiguity associated with analysis of variance models. , 1985, Electroencephalography and clinical neurophysiology.

[35]  E. Donchin,et al.  On quantifying surprise: the variation of event-related potentials with subjective probability. , 1977, Psychophysiology.

[36]  Leslie G. Ungerleider,et al.  A neural system for human visual working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[37]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[38]  Phillip J. Holcomb,et al.  Regulation of attention to novel stimuli by frontal lobes: an event‐related potential study , 1998, Neuroreport.

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

[40]  R. Knight,et al.  Neural Mechanisms of Involuntary Attention to Acoustic Novelty and Change , 1998, Journal of Cognitive Neuroscience.

[41]  Risto N t nen Attention and brain function , 1992 .

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

[43]  G. Holmes The prefrontal cortex: Anatomy, physiology, and neuropsychology of the frontal lobe (2nd ed.) , 1989 .

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

[45]  R. Knight Distributed Cortical Network for Visual Attention , 1997, Journal of Cognitive Neuroscience.

[46]  S. Yamaguchi,et al.  Anterior and posterior association cortex contributions to the somatosensory P300 , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[48]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. I. Superior temporal plane and parietal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[49]  E. Halgren,et al.  Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal lobe. , 1995, Electroencephalography and clinical neurophysiology.

[50]  Michael D. Rugg,et al.  The effect of attention on the P300 deflection elicited by novel sounds , 1995 .

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

[52]  Gregory McCarthy,et al.  Review : Functional Neuroimaging of Memory , 1995 .

[53]  R T Knight,et al.  Anatomic bases of event-related potentials and their relationship to novelty detection in humans. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[54]  R. Knight,et al.  P300 generation by novel somatosensory stimuli. , 1991, Electroencephalography and clinical neurophysiology.

[55]  E. N. Solokov Perception and the conditioned reflex , 1963 .

[56]  L. Kempe Handbook of Physiology. Section I. The Nervous System , 1982 .

[57]  E. Vurpillot,et al.  The development of scanning strategies and their relation to visual differentiation. , 1968, Journal of experimental child psychology.

[58]  J. Polich,et al.  Stimulus context determines P3a and P3b. , 1998, Psychophysiology.