Review
The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty

https://doi.org/10.1016/S0149-7634(01)00019-7Get rights and content

Abstract

A review of the literature that examines event-related brain potentials (ERPs) and novelty processing reveals that the orienting response engendered by deviant or unexpected events consists of a characteristic ERP pattern, comprised sequentially of the mismatch negativity (MMN) and the novelty P3 or P3a. A wide variety of evidence suggests that the MMN reflects the detection of deviant events, whereas the P3a is associated more with the evaluation of those events for subsequent behavioral action. On the scalp, the novelty P3a is comprised of at least two aspects, one frontal the other posterior, each with different cognitive (and presumably neurologic) correlates. Intracranial ERP investigations and studies of patients with localized brain lesions (and, to some extent, fMRI data) converge with the scalp-recorded data in suggesting a widespread neural network, the different aspects of which respond differentially to stimulus and task characteristics.

Introduction

Distinguishing between what is novel and what has already been experienced, or between degrees of novelty encompasses fundamental processes that enable one to appropriately react to stimuli in the environment. What is considered novel and/or salient depends also upon the context in which the eliciting event is encountered. For example, car honks while being a pedestrian are not as salient as those same environmental sounds when driving your car to work during rush hour. During the latter, it is a common experience for the driver to proceed from point A to point B without conscious awareness of how that stretch of highway was negotiated. The ‘noise’ outside as well as inside the automobile recedes into the background while focal attention is drawn to inner thoughts, or to the information conveyed by the radio. Yet, even while deep in thought, a biologically significant change in the background ‘noise’, such as a car horn or tire screech will cause a shift in attention i.e., an orienting response.

The orienting response [59], [87] is an involuntary shift of attention that appears to be a fundamental biological mechanism necessary for survival. Orienting is a rapid response to new (never experienced before), unexpected (out of context) or unpredictable stimuli, which essentially functions as a ‘what-is-it’ detector. Given the examples of the car horn and tire screech described above, the detection of the event precedes orienting and, if it is sufficiently deviant, engenders the involuntary capture of attention, enabling the event to enter consciousness, thus permitting an evaluation of the significance of the stimulus. This could lead, if the event is deemed significant, to behavioral action. The importance of this ubiquitous response can be seen from studies showing that human infants as young as 3 months old exhibit an orienting response to novel stimuli. For example, Kagan [46] demonstrated that infants oriented to the sudden onset of a female voice, while Fagan [22] showed that infants maintained their gaze for a longer time at novel stimuli when presented within a pair of novel and already viewed (i.e., familiar) stimuli.

Sokolov [87] demonstrated the plasticity of the orienting response by showing that stimuli which initially evoked the response no longer did so with repeated presentation. Habituation of the response is proposed to indicate that some type of memory for these prior events has been formed which modifies the response to the repeated incidences. It has been further proposed [88] that novel stimuli elicit processes that enable the construction of neural representations for these new events. As stimulus exposure continues and the neural representation is formed, the constructed representation is then continuously compared to incoming information. Habituation occurs when the representation matches sufficiently the external stimulus. Finally, future encounters with this, no longer novel, item will be facilitated.

Section snippets

Scope of this review

Orienting, habituation and memory processes for novel events have been measured physiologically and are the topics of the present review. The primary purpose of this review is to acquaint the reader with the state of knowledge concerning the temporal characteristics and neural substrates of the detection and evaluation of novel or unexpected events. As most of the physiological research regarding brain responses to novel events has been performed within the auditory modality, this review will

The scalp-recorded event-related brain potentials (ERPs)

ERPs are voltage fluctuations in the electroencephalogram (EEG) induced within the brain that are time locked to sensory, motor, or cognitive events. They provide a direct, non-invasive measure of the temporal course of the voltage changes that are extremely sensitive to manipulations of the cognitive context within which the eliciting stimuli are embedded. By contrast, the spatial resolution for identification of the neural sources generating these signals has been poor relative to the newer

Limitations of techniques for assessing the brain's novelty response

All of the techniques used to understand the brain's novelty response have their limitations, and these will be delimited here. However, the strengths of the different techniques can counterbalance the weaknesses when multiple techniques are used convergently to record brain activity in response to novel events. For example, the recovery of spatial information from the ERP waveform can be difficult, because for some ERP components there is no direct relation between the surface activity and the

Definition of ERP terms

Low frequency, deviant, events presented within a train of homogeneous stimuli elicit an orienting response. ERPs elicited by these same stimuli are comprised sequentially of the mismatch negativity (MMN) and the novelty P3, both of which will be described in detail in this review. Throughout the remainder of this paper we will use the term ‘novelty P3’ to refer to the P3 component elicited by events about which the subject has not been instructed prior to the experiment (e.g., environmental

ERP paradigms for studying ‘novelty’

Several methods have been devised to study the physiological antecedents and consequences of the orienting response within a laboratory setting. Perhaps the most often used paradigm is one that has been termed the Regular oddball task. By far, the vast majority of investigators have used the auditory modality, and much is known about the ERP correlates of orienting to deviant auditory events (see Refs. [70], [71] for detailed discussions). In a typical oddball experiment, two classes of stimuli

Physiological indices of the orienting response

The underlying physiology and neuroanatomical substrates of the brain's response to novel events has been assessed with a number of different methods, including (but not limited to) galvanic skin conductance [65], pupillary dilation [23], scalp-recorded ERPs [9], intracranially-recorded ERPs [6], and functional magnetic resonance imaging (fMRI) [74], and for various subject populations such as older adults [20], children [13], and patients with localized brain lesions [48].

Neural basis of the novelty response: functional MRI data

Some of the same neuroanatomical regions shown to contribute to the generation of the P3a by ERP methods have also been observed to show increased blood flow in hemodynamic studies conducted under similar experimental conditions. Unfortunately, to our knowledge, there is only one study that used complex, environmental stimuli (i.e., novels) [74]similar to those presented in the novelty oddball studies described earlier in this review. However, based on intracranial and lesion studies, common

Conclusions

This review makes it clear that multiple techniques will be required to understand more completely the temporo-spatial processing of novelty information by the brain. The fine-grained temporal information provided by scalp-recorded and intracranial ERP data converge in suggesting that the P3a component reflects a late stage of novelty processing, most likely related to the evaluative aspects of the orienting response. The excellent spatial resolution of fMRI combined with surface-recorded ERP

Acknowledgements

The authors thank Mr. Charles L. Brown, III for computer programming, Mr. Jeff Cheng, Mr. Martin Duff and Ms. Blanca Rancon for technical assistance. The authors thank Drs. Monica Fabiani and Victoria Kazmerski for contributions to some of the research reported here, and Dr Walter Ritter for a critical reading of a previous version of this manuscript. We also thank Dr Jennifer Mangels for her helpful comments. The authors acknowledge the help of Dr Cheryl Grady who provided them with the brain

References (102)

  • E. Halgren et al.

    Intracerebral potentials to rare target and distractor auditory and visual stimuli. II. Medial, lateral and posterior temporal pole

    Electroencephalogr Clin Neurophysiol

    (1995)
  • E. Halgren et al.

    Generators of the late cognitive potentials in auditory and visual oddball tasks

    Electroencephalogr Clin Neurophysiol.

    (1998)
  • D. Javitt et al.

    Demonstration of mismatch negativity in the monkey

    Electroencephalogr Clin Neurophysiol

    (1992)
  • R.T. Knight

    Decreased response to novel stimuli after prefrontal lesions in man

    Electroencephalogr Clin Neurophysiol

    (1984)
  • R.T. Knight et al.

    Contributions of temporal-parietal junction to the human auditory P3

    Brain Res

    (1989)
  • Z.J. Koles

    Trends in EEG source localization

    Electroencephalogr Clin Neurophysiol

    (1998)
  • J.D. Kropotov et al.

    Human auditory-cortex mechanisms of pre-attentive sound discrimination

    Neuroscience Letters

    (2000)
  • A. Mecklinger et al.

    Semantic aspects of novelty detection in humans

    Neurosci Lett

    (1997)
  • W. Miltner et al.

    A test of brain electrical source analysis (BESA): A simulation study

    Electroencephalogr Clin Neurophysiol

    (1994)
  • P. Pauli et al.

    Brain potentials during mental arithmetic: Effects of extensive practice and problem difficulty

    Cogn Brain Res

    (1994)
  • T. Rinne et al.

    Scalp-recorded optical signals make sound processing in the auditory cortex visible?

    Neuroimage

    (1999)
  • T. Rinne et al.

    Separate time behaviors of the temporal and frontal mismatch negativity sources

    Neuroimage

    (2000)
  • E. Schröger et al.

    Auditory distraction: event-related potential and behavioral indices

    Clin Neurophysiol

    (2000)
  • J.P. Wikswo et al.

    The future of the EEG and MEG

    Electroencephalogr Clin Neurophysiol

    (1993)
  • C. Alain et al.

    Human intracerebral potentials associated with target, novel, and omitted auditory stimuli

    Brain Topogr

    (1989)
  • K. Alho et al.

    Processing of novel sounds and frequency changes in the human auditory cortex: Magnetoencephalographic recordings

    Psychophysiology

    (1998)
  • J.A. Ballas

    Common factors in the identification of an assortment of brief everyday sounds

    J Exp Psychol Hum Percept Perform

    (1993)
  • G.S. Berns et al.

    Brain regions responsive to novelty in the absence of awareness

    Science

    (1997)
  • V.P. Clark et al.

    Responses to rare visual target and distractor stimuli using event-related fMRI

    J Neurophysiol

    (2000)
  • Y.M. Cycowicz et al.

    developmental study of repetition priming by auditory novel stimuli

    Psychophysiology

    (1996)
  • K.R. Daffner et al.

    Disruption of attention to novel events after frontal lobe injury in humans

    J Neurol Neurosurg Psychiat

    (2000)
  • K.R. Daffner et al.

    The central role of the prefrontal cortex in directing attention to novel events

    Brain

    (2000)
  • L.Y. Deouell et al.

    Mismatch negativity in dichotic listening: evidence for interhemispheric differences and multiple generators

    Psychophysiology

    (1998)
  • E. Donchin et al.

    Novelty P3 is not a shifty P3

    Psychophysiology

    (1999)
  • J. Downar et al.

    A multimodal cortical network for the detection of changes in the sensory environment

    Nat Neurosci

    (2000)
  • C. Escera et al.

    Neural mechanisms of involuntary attention to acoustic novelty and change

    J Cog Neurosci

    (1998)
  • Fabiani, M., Friedman, D. Changes in brain activity patterns in aging: the novelty oddball. Psychophysiology,...
  • M. Fabiani et al.

    Naming norms for brief environmental sounds: Effects of age and dementia

    Psychophysiology

    (1996)
  • Fagan JF. The paired-comparison paradigm and infant intelligence. In: Diamond A, editor. The development and neural...
  • D. Friedman et al.

    Event-related potential (ERP) studies of memory encoding and retrieval: a selective review

    Microsc Res Tech

    (2000)
  • D. Friedman et al.

    Effects of aging on the novelty P3 during attend and ignore oddball tasks

    Psychophysiology

    (1998)
  • H.R. Friedman et al.

    Coactivation of prefrontal cortex and inferior parietal cortex in working memory tasks revealed by 2DG functional mapping in the rhesus monkey

    J Neurosci

    (1994)
  • H. Gaeta et al.

    An event-related potential evaluation of involuntary attentional shifts in the young and elderly

    Psychol Aging

    (2001)
  • A. Gevins et al.

    Electroencephalographic imaging of higher brain function

    Philos Trans R Soc Lond B Biol Sci

    (1999)
  • M.H. Giard et al.

    Brain generators implicated in the processing of auditory stimulus deviance: A topographic event-related potential study

    Psychophysiology

    (1990)
  • O. Godefroy et al.

    Novel decision making in patients with prefrontal or posterior brain damage

    Neurology

    (1997)
  • P.S. Goldman-Rakic

    Circuitry of primate prefrontal cortex and regulation of behavior by representational memory

  • P.S. GoldmanRakic

    Working memory and the mind

    Sci Am

    (1992)
  • E. Halgren et al.

    Endogenous potentials generated in the human hippocampal formation and amygdala by infrequent events

    Science

    (1980)
  • H.J. Heinze et al.

    Combined spatial and temporal imaging of brain activity during visual selective attention in humans

    Nature

    (1994)
  • Cited by (1046)

    View all citing articles on Scopus
    View full text