Habituation: an event-related potential and dipole source analysis study

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Abstract

The goal of this study was to investigate habituation processes in the brain, and in particular, to identify the brain structures involved in these processes. Therefore, event-related potentials (ERPs) were recorded in response to a series of repeated, task-irrelevant, salient stimuli presented against the background of a cognitive task which required the subjects to attend to a fixation sign on a TV screen. Stimuli were presented randomly in one of four possible quadrants of the TV screen. Dipole analyses were performed in order to localize the source of stimulus repetition effects (habituation). As expected, there was a decrease in amplitude of the N1 and P3 components as a function of stimulus repetition; habituation of N1 occurred faster than that of the P3 component. It is suggested from the results of dipole analyses that the N1 effect concerns diffuse cortical activation. The P3 habituation effect seemed to involve the temporal cortex especially.

Introduction

Decrease of response amplitude as a function of stimulus repetition is one of the basic properties of the Orienting Response (OR) (Siddle et al., 1983). This property has been demonstrated for the skin conductance reaction (SCR). Some components of the event-related potential (ERP) have also been found to decrease to repeatedly presented stimuli (Rust, 1977, Wastel and Kleinman, 1980, Barry et al., 1992, Geisler and Polich, 1994, Kazmerski and Friedman, 1995, Cycowicz et al., 1996, Romero and Polich, 1996, Cycowicz and Friedman, 1997, Friedman et al., 1998, Ravden and Polich, 1998). Verbaten et al. (1986) and Kenemans et al. (1989) showed that the N1 and P3 components particularly decrease in amplitude as a function of stimulus repetition. However, there appears to be a pronounced difference in speed of habituation between the two ERP components. Verbaten et al. (1986) found that the decrease in the amplitude of the vertex N1 was much faster than that of P3. Furthermore, the latter authors reported that the vertex N1 and the skin conductance reaction habituated equally fast under non-signal (=task-irrelevant) conditions. These data of Verbaten et al. (1986) suggest that the vertex N1 is involved in a more crude type of stimulus processing than the P3 vertex. According to the most influential current hypothesis about the psychological significance of P3, in the context updating hypothesis (Donchin, 1981, Donchin and Coles, 1988), P3 reflects the updating of a proper representation of the environment in memory. It has to be acknowledged here, however, that alternative interpretations of P3 exist, such as the hypothesis of Verleger (1988) (see also Verleger, 1998), in which P3 is assumed to be elicited by stimuli that close a (meaningful) context (context closure instead of context updating).

The first aim of the present study was to try to replicate the fast habituating N1 effect and furthermore, to determine the neural sources involved in this effect by using the BESA dipole approach (Scherg, 1990, Scherg and Picton, 1991).

The second purpose of this study concerned the P3 component and its habituation. In current theories about visual information processing, posterior-cortical structures play an important role in that a dorsal pathway to the parietal cortex concerned with spatial information is distinguished from a ventral pathway to the inferior temporal cortex concerned with non-spatial information (e.g. Mishkin et al., 1983, Livingstone and Hubel, 1988, Zeki and Ship, 1988, Desimone and Ungerleider, 1989, Kandel, 1991). It may be assumed that both spatial and non-spatial stimulus information are part of the ‘neuronal model’ (Sokolov, 1963), are updated in memory (Donchin, 1981, Donchin and Coles, 1988; see however, Verleger, 1988) during repeated stimulus presentation, and are reflected in the P3 component. If the non-spatial properties (identity) of the stimuli are constant, and the location of the stimuli varies randomly, it may be expected that habituation will occur faster in brain structures involved in identity processing, i.e. along the ventral route (e.g. the inferior temporal cortex) than in structures (sources) involved in location processing (the dorsal route). This question was investigated by applying the BESA approach to ordinally averaged ERPs (see also Ritter et al., 1968).

Section snippets

Subjects

Eight healthy college students (5 female and 3 male) aged between 19 and 24 years (mean age 22.3 years) served as paid volunteers in this experiment. They all had normal or corrected-to-normal vision.

Apparatus and stimuli

Subjects were seated in a dimly-illuminated, sound attenuated, electrically shielded room, facing a color-video monitor. They were presented with 384 trains of stimuli. Because the present study was about habituation effects on the ERPs, it had to be ascertained that in each train unique standard

Results

In Fig. 1 the average ERPs in response to the first and the eighth standard in a series of novelty stimuli are shown. The ERPs elicited by these stimuli in the lower visual hemifield consisted of a positive component peaking at approximately 100 ms (P1), a negative component peaking at approximately 150 ms (N1), and a prolonged positivity. For upper visual hemifield stimuli the same sequence of components was seen in the ERPs, but the peak latency of the early positive (P1) and negative (N1)

Discussion

As expected, there was a decrease in the amplitudes of the N1 (160–200 ms) and the P3 (from 320 ms on) components in response to repeated standards.

References (37)

  • R Romero et al.

    P3(00) habituation from auditory and visual stimuli

    Physiol. Behav.

    (1996)
  • M.N Verbaten et al.

    Processing capacity and the frontal P3

    Int. J. Psychophysiol.

    (1997)
  • M.N Verbaten et al.

    Habituation of early and late visual ERP components and the orienting reaction: the effect of stimulus information

    Int. J. Psychophysiol.

    (1986)
  • Bruin, K.J., Kenemans, J.L., Verbaten, M.N., Van der Heijden, A.H.C., in prep. Processing of visual deviance: an...
  • Brunia, C.H.M., 1997. Op het kruispunt van anticipatoire attentie en motorische preparatie. In: Kok, A., Boelhouwer,...
  • Y.M Cycowicz et al.

    An ERP developmental study of repetition priming by auditory novel stimuli

    Psychophysiology

    (1996)
  • R Desimone et al.

    Neural mechanisms of visual processing in monkeys

  • E Donchin

    Surprise!... Surprise?

    Psychophysiology

    (1981)
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