International Journal of Psychophysiology 47 (2003) 187–198

Preferred EEG brain states at stimulus onset in a fixed

interstimulus interval auditory oddball task, and their effects on
ERP components
Robert J. Barrya,*, Vilfredo de Pascalisb, Darren Hoddera, Adam R. Clarkea,
Stuart J. Johnstonea
a
Brain & Behaviour Research Institute and Department of Psychology, University of Wollongong, Wollongong 2522, Australia
b
Dipartimento di Psicologia, Universita di Roma, 00185 Rome, Italy

Received 7 May 2002; received in revised form 16 October 2002; accepted 21 October 2002

Abstract

Previous work has indicated the importance of ongoing EEG activity in the elicitation of the event-related potential
(ERP), supporting the conceptualisation of the ERP in terms of amplification and attenuation of component
frequencies in the EEG. We investigated the importance of the phase of narrow-band EEG activity in generating N1
and P2 components in the auditory ERP. An auditory oddball paradigm requiring a button-press response to targets,
with fixed interstimulus interval (ISI) and 15% target probability, was utilised. The continuous EEG at Cz was
recorded from 16 subjects as the raw data set. Offline digital filtering was used to separate the EEG into 13 narrow
bands from 1 to 13 Hz. For each band, the phase at the onset of each non-target stimulus was determined. These
were used to sub-average the unfiltered data stream at each of four phases for each of 13 frequencies for each subject.
Phase effects were examined in terms of two orthogonal dimensions of electrical brain activity: Cortical negativity
and negative driving. Stimulus onset varied as a function of these dimensions in a non-random fashion across
frequency, indicating the preferential occurrence of particular phases, interpretable as preferred brain states. Large
differential effects were also apparent in N1 and P2 amplitudes. These data indicate important aspects of brain
dynamics, suggesting that in a fixed-ISI paradigm the component frequencies of the EEG are dynamically adjusted
in order to provide particular brain states at stimulus occurrence to facilitate the brain’s processing of the stimulus.
䊚 2002 Elsevier Science B.V. All rights reserved.

Keywords: EEG; Auditory ERP; EEG Phase; Narrow-band filtering; Brain dynamics

1. Introduction tations of that stimulus. Averaging is necessary to

The event-related potential (ERP) elicited by a
stimulus is actualised as the averaged time-locked
electrophysiological response to repeated presen-
*Corresponding author. Tel.yfax: q61-2-4221-4421.
E-mail address: robert_barry@uow.edu.au (R.J. Barry).
increase the signal:noise ratio of the small stimu-
lus-related response hidden in the background EEG
activity, by removing the random EEG ‘noise’.
There are a number of problems with this simple
conceptualisation, which may be overlooked in
common discussion. The first of these is with the

0167-8760/03/$ - see front matter 䊚 2002 Elsevier Science B.V. All rights reserved.
PII: S 0 1 6 7 - 8 7 6 0 Ž 0 2 . 0 0 1 5 1 - 4
188 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198
concept of the ERP itself. This ERP has no
concrete existence outside the average which
formed it, yet it sometimes appears to be concep-
tualised as the response to each stimulus. Perhaps
the average does not provide a good estimate of
the trial-to-trial response, which could well be
highly variable (e.g. Anderson et al., 1991; Ford
et al., 1994). The second problem is with the
concept of the EEG itself. If the ongoing EEG is
considered as background ‘noise’, and hence a
problem to be eliminated in the averaging process,
the possibility that the ongoing EEG plays a
fundamental role in the genesis of the ERP may
be overlooked.
An alternative conceptualisation is to explicitly
recognise that the average ERP is just that—an
average—and that this average says little about
the brain’s response to any individual stimulus.
The responses to individual stimuli may vary
widely, perhaps largely depending on the nature of
the EEG at stimulus onset. At the cellular level,
this has been demonstrated by Arieli et al. (1996).
Using visual stimulation in cat, these authors
concluded that ‘the processing of sensory input in
the visual cortex involves the combination of a
deterministic response and ongoing network
dynamics’ (p. 1870). Further, Makeig et al. (2002)
recently described the human ERP to non-target
stimuli in a visual selective-attention task in terms
of its generation by ‘partial stimulus-induced
phase-resetting of multiple electroencephalograph-
ic processes’ (p. 690). In this alternative concep-
tualisation, the ‘background’ EEG activity is seen
as exquisitely reflecting the brain’s momentary
state of activity, and subtly determining the
response to the stimulus, as reflected in both
behavioural and ERP outcomes (Basar, ¸ 1980).
Supporting evidence for this approach is provided
by studies of the effect of stimulus presentation in
particular brain states. For example, there has been
a substantial number of studies examining the
effect of differences in the amplitude of particular
EEG frequencies in the prestimulus period upon
ERP components (e.g. Barry et al., 2000; Basar ¸ these frequencies. This appears to be compatible
and Stampfer, 1985; Basar ¸ et al., 1989, 1998;
Brandt, 1997; Brandt and Jansen, 1991; Brandt et
al., 1991; Jasiukaitis and Hakerem, 1998; Price,
1997; Rahn and Basar,¸ 1993).
Perhaps the most widely studied frequency
range in these reports has been the alpha band. In
a recent study, Barry et al. (2000) concluded that
amplitudes of both the N1P2 and N2P3 complexes,
elicited by targets in an auditory oddball paradigm,
were directly proportional to prestimulus RMS
alpha amplitude—i.e. these components are larger
when stimuli are presented during high-amplitude
alpha states. These data supported the previous
findings of Brandt’s group with N1P2, and Jasiu-
kaitis and Hakerem (1998) with P3. Barry et al.
(2000) noted that contradictory reports of
enhanced ERP components with lower levels of
prestimulus alpha, and vice-versa, often appeared
to be associated with paradigms in which stimuli
were selectively presented when subjects were in
particular states (e.g. Basar¸ et al., 1998; Price,
1997; Rahn and Basar,¸ 1993). Such paradigms are
markedly different from common ERP studies,
which instead present stimuli on a scheduled basis
independently of fluctuations in the momentary
state of the subject. It is the effect of prestimulus
EEG state in the latter type of experiment which
constitutes the present focus of our work.
Although the relationships between prestimulus
alpha and the N1 and P3 ERP peaks have been
widely explored, a few other EEG frequencyyERP
component linkages have also been examined. For
example, Stampfer and Basar ¸ (1985) concluded
that the ‘N100 peak is formed mainly by 3.5–8
Hz, and 8–13 Hz activity; the P200 peak is formed
by the superposition of the first peak of 1–3.5 Hz
activity and the first positive peak of 3.5–8 Hz
activity’ (p. 187). Basar
¸ et al. (1984) concluded
that ‘the endogenous N100 wave is related to the
alpha activity, and« waves with latencies higher
than 300 ms are related to activities in the theta
and delta frequency range’ (p. 19). Kolev and
¨
Schurmann (1992) confirmed the important role
of theta and alpha oscillations in the formation of
ERPs in a non-response single-stimulus paradigm,
essentially confirming the dependence of the com-
ponents of the N1P2 complex on modulation of
with a study by Brandt et al. (1991), which
reported that N1P2 amplitudes produced by visual
stimuli presented with a quasi-random interstimu-
lus interval (ISI) were directly related to presti-
 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198
mulus alpha amplitude, and inversely related to
prestimulus delta and theta amplitudes. There was
no relation with beta activity. Over all bands,
prestimulus power predicted some 45% of the total
¸
variance in N1P2 amplitude. Basar-Eroglu et al.
(1992) and Demiralp and Basar ¸ (1992) explored
this further, noting that delta and theta activity
seemed important in relation to late ERP compo-
nents in the oddball task (presumably the P3)
while theta activity appeared important in relation
to early components (presumably the N1P2 com-
plex) in a stimulus omission study. Basar ¸ et al.
(1998) discussed earlier in relation to alpha activ-
ity, also explored the impact of prestimulus theta
in elicitation of the visual evoked potential. Yor-
danova and Kolev (1996, 1997) and Yordanova et
al. (1996) have reported further work on the
development of the theta-P3 relationship with chil-
dren and adults. That is, studies to date have found
that activity in the delta, theta, and alpha EEG
frequency ranges affect ERP components, but fre-
quencies beyond the alpha range appear to have
little direct involvement in the generation of the
major ERP components.
Embedded in many of the reports cited above,
particularly those from the Basar ¸ group, is the
suggestion that with regular stimuli, phase adjust-
ments occur in the prestimulus EEG. For example,
¸ and Stampfer (1985) reported that, in a
Basar
fixed-ISI paradigm with alternating target and non-
target stimuli, the delta activity before target stim-
uli shows ‘evidence of a stable phase-reordering
or ‘preferred phase angle’, at the point of stimu-
lation. In the examples shown, there is evidence
of a maximum negativity at the time of stimula-
tion’ (p. 167). In the same study, alpha activity
was also ‘associated with increasing phase align-
ment at the point of stimulation’ (p. 170), and a
figure suggests that this also involved a preferential
occurrence of EEG negativity; further, the subse-
quent alpha peak appears to largely determine the
timing of the N1 component. Such observations
led them to conclude that ‘a regular pattern of
stimulation can induce a ‘preferred’ phase angle,
which appears to facilitate an optimal brain
response to the sensory input’ (p. 175). Similar
findings were presented by Basar ¸ et al. (1984) in
a study which presented tones at 1 s ISIs and
189
omitted every third or fourth tone, leading them to
state that ‘phase-reordering at the time of stimulus
omission is due to the behavioural state resulting
from the application of repetitive stimuli’ (p. 9).
The importance of such a preferred phase
appears to arise from its impact on functional
aspects of brain state and behaviour. For example,
´
Remond (1969) demonstrated that the phase of
alpha activity at stimulus onset was important in
determining the amplitude and topography of the
subsequent alpha activity. Other early work (e.g.
Callaway and Yeager, 1960; Dustman and Beck,
1965; Trimble and Potts, 1975) concentrated on
the differential effects of stimulation at negative
and positive peaks of the alpha cycle. Generally,
maximum excitability occurred when stimuli were
presented at negative peaks, an effect apparent in
both ERP components and reaction time measures.
Such findings appear to interleave with other work
which links cortical negativity with increased brain
excitability (e.g. Pleydell-Pearce, 1994; Rockstroh
et al., 1989). Together they suggest that, at least
within fixed-ISI paradigms, the brain reorders the
phase of its alpha activity, and perhaps other
frequencies, to preferentially display negativity at
stimulus onset, and that this optimises its excita-
bility and hence affects behavioural and ERP
outcomes.
Jansen and Brandt (1991) investigated the
effects of alpha phase using visual stimulation
presented at irregular intervals, with no task requi-
rements. They used 1000 stimuli with ISIs varying
from 2 to 6 s, and divided the prestimulus alpha
cycle into eight phases. Generally, alpha activity
was found to continue into the poststimulus period,
and the first or second negative peak was identified
with the N1. Its amplitude and latency varied
substantially with alpha phase at stimulus onset.
N1 was found to be maximum when stimulus
onset was near a positive-going zero crossing.
Smaller effects were obtained in relation to the
P2, which was considered to be related to partial
blocking of the alpha activity. Unfortunately, this
interesting study presented data from only 5 sub-
jects, and it is unclear how these individual results
can be generalised. Also, the study employed an
eyes-closed condition, which, together with the
absence of a task, would be expected to result in
190 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198
relatively high alpha amplitudes. Phase determi-
nation was then restricted to selected 1 s presti-
mulus epochs with high alpha level ()100 mV).
This high level of alpha activity further limits the
generalisability to common ERP paradigms. More
importantly, their phase determination was based
on peak and trough identification in the EEG
(bandwidth 0.032–35 Hz, which was ‘smoothed’
with an unspecified filter), and trials were accepted
if the period of the cycle used to determine phase
corresponded to a frequency between 5 and 20 Hz.
This extension beyond the normal alpha limits
makes interpretation of the results extremely
problematic.
More recently, Brandt (1997) confirmed that
poststimulus filtered alpha was enhanced when
stimuli were presented in the half-cycle associated
with a positive rather than a negative zero-crossing.
This means that stimuli presented in the half cycle
between a prestimulus negative peak and the fol-
lowing positive peak were most influential in
generating an enhanced negativity approximately
100 ms poststimulus onset, activity presumed to
underly the N1. Unfortunately, Brandt examined
these poststimulus effects only in terms of the
alpha frequency range rather than the broad-band
ERP itself. Thus, while these studies have served
to illustrate that EEG phase at stimulus onset is an
important characteristic influencing the brain’s
response, a systematic exploration of the effects of
phase is lacking.
One of the impediments to research investigating
phase effects is the difficulty of conceptualising,
measuring, and analysing the phase of a frequency
component as an independent variable in the
experimental paradigm. For example, Brandt
(1997) used the approach of Winfree (1987) to
investigate the occurrence of phase-resetting at
stimulus onset. This is a highly mathematical
approach which appears useful in the detection
and description of the phenomenon of phase-
resetting rather than an understanding of its func-
tional role in ERP and behavioural outcomes. In
another approach, Haig and Gordon (1998b) intro-
duced the use of angular or circular statistics to
handle phase measures, and used this approach to
relate ERP outcomes to prestimulus alpha phase
synchronicity, defined in terms of reduced phase
variability across five occipito-parietal sites. Larger
N100s and shorter reaction times were obtained
when prestimulus alpha phase synchronicity was
high. Unfortunately, this measure appears to be
confounded with alpha amplitude, in that highly
synchronised alpha in the occipito-parietal region
is likely to be of high amplitude. It is thus unclear
whether a measure of phase synchronicity has
potential value independently of prestimulus
amplitude or power measures. In a later study
further exploring the use of circular statistics in
this field, Haig and Gordon (1998a) established,
in a fixed-ISI auditory oddball paradigm, that
single-trial target ERPs which had a detectable P3
component differed from those which did not, in
terms of the mean alpha phase at stimulus onset.
Some three in four trials had P3s, and their mean
phase at stimulus onset was late in the period
Brandt (1997) referred to as ‘positive zero
crossing’, while the one in four trials without P3s
had mean phase at stimulus onset earlier in the
same period. However, their topographic analysis
used averages with and without P3s, and their
corresponding mean alpha phases at stimulus
onset, which were defined independently at each
site, making it difficult to speculate on any under-
lying mechanisms.
The current work adopted a different approach
to the measurement of phase, in an effort to
facilitate the relating of phase measures to a wider
range of concepts which appear useful in this
arena. Fig. 1 shows a simple sine wave, drawn
with negative up in order to relate to common
ERP conventions, with 4 phase divisions at inter-
vals of py2. Phases B and C subdivide Brandt’s
(1997) ‘positive zero crossing’ period, while D
and A correspond to his ‘negative zero crossing’
period. Haig and Gordon’s (1998a) phase measure
was defined in terms of 08 at a positive peak and
1808 at a negative peak, so that Phase A corre-
sponds to their range of 90–1808. Rather than
work with such mathematically defined divisions
as independent variables, an attempt was made
here to relate them to more intuitively meaningful
physical concepts, so that their effects on ERP
measures could be better explored. Thus, this study
investigated two easily conceptualised physical
variables. Cortical negativity can be examined in
 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198
Fig. 1. Definition of the four phases of the EEG waveform
used in this study.
the comparison of the effects of (AqB) vs. (Cq
D). This represents perhaps the earliest aspect of
research into phase effects, investigated by pre-
senting stimuli at the negative or positive peaks of
alpha waves. A second physical variable, negative
driving, can be examined in the comparison of
(AqD) vs. (BqC). This relates to the nature of
the changing of the cortical negativity variable—
is it increasing (phases A and D) or decreasing
(phases B and C)? Negative driving covers
Brandt’s ‘negative zero crossing’ vs. ‘positive zero
crossing’ effects. Note that both (AqD) and (Bq
C) cover negative and positive phases, and hence
effects of negative driving are independent of the
effects of cortical negativity.
Although some of these studies have used Fast
Fourier Transforms (FFTs) to obtain spectral infor-
mation regarding prestimulus EEG (e.g. Brandt
and Jansen, 1991), many have employed band-
pass filtering of the EEG on a trial-by-trial basis.
These have used either traditional band definitions
(e.g. 8–13 Hz alpha: Barry et al., 2000; Brandt,
1997; Haig and Gordon, 1998a,b) or closely relat-
ed bands derived from peaks in the individual’s
amplitude–frequency characteristic curve (e.g.
Basar
¸ et al., 1984). The present study aimed to
pursue this issue with very narrow-band (1 Hz
bandwidth) digital filtering. This was an attempt
to pass beyond the limits of the traditional EEG
191
bands, which may constrain the interpretation of
the EEGyERP relationship. One potential problem
with any narrow-band filtering approach is ‘ring-
ing’ in the filter. This refers to an unplanned and
unwanted high level of amplification which may
occur with frequencies near the turning points of
the filter. An ideal filter has an amplification of 1
in the pass band, and 0 beyond. Real filters have
amplification ripples in the pass band, which may
be relatively large near the cut-off frequencies,
leading to ‘ringing’. It was suggested by Brandt
and Jansen (1991) and Barry et al. (2000) that
some of the conflicting data apparent with the
examination of alpha frequency effects using dig-
ital filtering may have been caused by ‘ringing’.
Barry et al. (2000) specifically checked their alpha
filter characteristics with white noise to ensure that
‘ringing’ was not a problem in that study.
Thus the present study investigated the occur-
rence of different phases of EEG activity at stim-
ulus onset in a fixed-ISI auditory oddball task, at
frequencies up to, and including, the alpha range.
We also examined their effects on the amplitude
of ERP components. Because we sub-averaged
ERPs in terms of phase at stimulus onset, only the
responses to the more-numerous background stim-
uli in the oddball task could be examined. This
effectively limited analysis to the N1 and P2
components. Effects in these components were
derived by examining narrow-band filtered EEG,
in 1 Hz bands, in terms of the four phase periods
defined above, and analysing the occurrence of
these brain states and the subsequent ERP out-
comes in terms of the different combinations of
phases representing variation in the variables of
cortical negativity and negative driving defined
above.
2. Materials and methods
2.1. Subjects
Sixteen undergraduate subjects (11 females, 5
males), aged between 19 and 47 years, participated
in this study as one means of satisfying a course
requirement in Psychology. All claimed normal
hearing, and gave written informed consent in
accordance with a protocol approved by the Uni-
192 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198
versity of Wollongong Human Research Ethics
Committee.
2.2. Procedure
Continuous EEG was recorded from 17 scalp
sites using an electrode cap with tin electrodes,
referenced to linked ears, with a gain of 50 000, a
time constant of 5 s, and upper cut-off frequency
of 35 Hz. Vertical EOG (VEOG) was recorded,
from electrodes above and below one eye, with a
gain of 20 000. All impedances were below 5 kV.
Data were continuously sampled at 256 Hz and
stored for off-line analysis.
Subjects sat in a reclining chair in an air-
conditioned sound-reduced room separate from the
recording equipment. Each subject participated in
two blocks of an auditory oddball task with 15%
target probability. Each block contained a random
mix of 102 standard (background) stimuli of 1000
Hz and 18 deviant (target) stimuli at 1500 Hz. ISI
was fixed at 1300 ms. All stimuli were 40 ms
duration with 16 ms riseyfall times and presented
via circumaural headphones at 80 dB SPL. A
button-press response to the target was required.
During this task, subjects were requested not to
blink, and to remain fixated on a small cross on a
computer monitor.
2.3. EEG post-processing
Only Cz data from the 204 background stimuli
presented to each subject were analysed for this
study. Trials with button-presses or ocular artifact
(VEOG)100 mV) were rejected. For each 1 Hz
band from 1 to 13 Hz, the recorded EEG was
passed through a narrow-band finite-impulse
response digital filter, and the signal phase-shift
was adjusted to 0. Testing with white noise con-
firmed that the pass-band of each filter was centred
at its nominal frequency, with 3 dB reduction at
"0.5 Hz, 17 dB reduction at "1.0 Hz and 024
dB at and beyond "1.5 Hz. There was no sugges-
tion of ringing in any set of filter characteristics.
For each filter band, for each non-target stimu-
lus, the phase at stimulus onset was determined
using the four ranges defined in Section 1. This
determination involved the evaluation of two par-
ameters of each filtered data stream at the instant
of each stimulus onset: (1) whether the voltage
was negative (A or B) or positive (C or D), and
(2) whether the slope (first derivative) of the
voltage versus time signal was negative (A or D)
or positive (B or C). These four phases were then
used to ‘bin’ or sub-average the unfiltered (wide-
band) EEG segments associated with each stimu-
lus. This formed four averaged wide-band ERPs
differing in narrow-band phase at stimulus onset,
for each of the 13 narrow frequency bands, for
each subject.
For each subject, FFTs of 1 s raw EEG epochs
centred at stimulus onset were averaged for the
acceptable epochs (VEOG-100 mV, no button-
press) for non-target stimuli, in order to evaluate
the frequency composition within the 1–13 Hz
range. This allowed an estimation of the relative
importance of phase effects at different frequencies
in determining the ERP outcomes. The occurrence
of each phase at stimulus onset was examined as
a function of frequency to investigate the occur-
rence of preferred brain states in this paradigm.
The averaged ERPs at each phase were used to
determine N1 and P2 amplitudes relative to a 200
ms prestimulus baseline period, and these were
examined as a function of phase at each frequency.
2.4. Statistical analyses
The dependent variables of interest were the
proportion of stimulus events which occurred in
each phase range, and the amplitudes of N1 and
P2. The first of these addressed the question of
preferred brain states, and was examined using
proportions tested with the binomial test. The
impact of these phases on each of the ERP com-
ponents was examined using paired t-tests. Activity
as a function of phase was explored in terms of
two orthogonal factors: Cortical negativity—phas-
es AqB vs. CqD, and negative driving—phases
AqD vs. BqC. Because of the number of tests
used (phase effects tested at each of 13 frequen-
cies), the Bonferroni correction was employed for
all significance tests.
3. Results
The number of ERP responses accepted from
the 204 background stimuli ranged across the 16
 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198 193

Fig. 3. Mean power at each frequency relative to that at 1 Hz.

Fig. 2. Grand mean ERP at Cz.

subjects from 60 to 140, with a mean of 102.2

(S.D.s18.6). The mean ERP to these background
stimuli, averaged across subjects, is shown in Fig.
2. Prior to stimulus onset, a CNV of some y1.7
mV is apparent, developing substantially in the
200 ms immediately before stimulus onset. There
is a marked N1, with amplitude of y6.3 mV and
mean latency approximately 90 ms, followed by a
clear P2 with amplitude 2.2 mV at 220 ms.
FFTs of 1 s epochs centred on stimulus onsets
for the accepted epochs were converted to relative
power in terms of that in the 1 Hz bin, and the
average across subjects is shown across the 1–13
Hz range in Fig. 3. These data indicate the impor-
tance of low frequency data, particularly in the 1–
3 Hz delta band, relative to higher frequencies, in
these epochs.
An example of phase binning for a representa-
tive subject (S1), with means for the 1 Hz filtered
data stream, is shown in the top panel of Fig. 4.
Note the appearance of large amplitude 1 Hz
activity, as indicated to occur generally in Fig. 3.
Also note how the procedure successfully identi-
fied and separated the filtered 1 Hz activity into
four phase ranges matching the specifications of
Fig. 1. The bottom panel of Fig. 4 shows the
corresponding unfiltered broad-band data stream
from this subject, separated into four sub-averages
on the basis of the 1 Hz phase at stimulus onset. Fig. 4. Filtered 1 Hz EEG activity for S1 separated by phase
For this 1 Hz example, the prestimulus CNV is (A, B, C, D) at stimulus onset (top panel) and the correspond-
apparent only in the ERPs associated with stimulus ing mean broad-band ERPs (bottom panel).
194 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198

(alpha), with the converse apparent at 4, 5 and 6

Hz (theta). With negative driving, negative-going
phases occurred significantly more often than pos-
itive-going phases at 3 and 4 Hz (spanning delta
and theta), and at 13 Hz (alpha), with the converse
effect at 6, 7, 8 and 9 Hz (spanning the theta and
alpha bands).
The amplitude of the N1 and P2 components
both varied significantly as a function of phase at
stimulus onset, and differentially as a function of
frequency. Fig. 6 (top panel) shows that with
cortical negativity, N1 amplitude was significantly
reduced if stimuli occurred in negative phases at
2, 3, 4 and 5 Hz (delta and theta bands), but
increased if stimuli occurred in negative phases at
9 and 10 Hz (alpha band), relative to the effects
of stimulus presentation in positive phases at those

Fig. 5. Occurrence of different phases at stimulus onset for

each frequency band, separated in terms of cortical negativity
(top) and negative driving (bottom).

presentation during phases A and B. These phases

also seem to be associated with a much larger
N1P2 complex than phases C or D.
Across subjects there were marked differences,
as a function of frequency, in the occurrence of
the different phases. The two panels in Fig. 5
indicate the proportion of stimuli which occurred
as a function of cortical negativity and negative
driving, with significant differences indicated. If
there were no preferred brain states at stimulus
onset in this task, i.e. if phase at stimulus onset
occurred by chance, we would expect 50% of trials
to fall in each category of the two experimental
variables. This is clearly not the case with either
of these variables. With cortical negativity, nega-
tive phases occurred significantly more often than Fig. 6. N1 amplitude as a function of cortical negativity (top)
positive phases at 2 Hz (delta), and 10 and 11 Hz and negative driving (bottom) at each frequency.
 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198
Fig. 7. Amplitude of P2 as a function of cortical negativity
(top) and negative driving (bottom) at each narrow-band
frequency.
frequencies. For negative driving, Fig. 6 (bottom
panel) indicates that negative-going phases pro-
duced much larger N1 amplitudes than positive-
going phases at 1, 2 and 3 Hz (delta), and 4 and
5 Hz (theta), with the converse but smaller effect
at 7 Hz (theta) and 9 Hz (alpha).
Fig. 7 (top panel) shows that the amplitude of
the P2 component was markedly affected by cor-
tical negativity at low frequency, being much larger
for stimuli presented at negative phases than at
positive phases for 1, 2 and 3 Hz (delta). There
were no cortical negativity effects at higher fre-
quencies. With negative driving, P2 was much
reduced for stimuli presented during negative-
going phases at 1 and 2 Hz (delta), and also
195
reduced at 5 and 6 Hz (theta), relative to presen-
tation during positive-going phases (Fig. 7, bottom
panel).
4. Discussion
4.1. Preferential brain states
Across the frequency range explored, there were
marked differences in the occurrence of different
phases at stimulus onset. Cortical negativity
occurred preferentially in both the delta (from 1
to 3 Hz, but reaching significance at 2 Hz) and
alpha (at 10–11 Hz) bands, with the opposite
effect apparent in the 4–6 Hz theta range. The
size of this last effect is particularly substantial,
with cortical negativity occurring in only 1y3 of
the epochs. The preferential occurrence of cortical
negativity in the delta and alpha ranges confirms
the observations of Basar¸ and Stampfer (1985).
The relative power distribution across the epochs
examined (Fig. 3), with greater power at lower
frequencies, suggests that the low frequency delta
effect is most important. This low-frequency phase
reordering, leading to a preferential occurrence of
cortical negativity in the delta range, appears to
underlie the substantial CNV noted in these data.
This link is suggested by Fig. 2, which indicates
that the quarter-period of the CNV component in
these ERP data is approximately 200 ms, indicat-
ing a frequency equivalent of 1–2 Hz. The gen-
eration of the CNV may simply reflect the
preferential occurrence of cortical negativity, with
the attendant excitabilityyactivation providing an
important element in the mechanism underlying
the proposed facilitation of the ‘optimal brain
response’ (Basar
¸ and Stampfer, 1985).
Cortical negative driving, defined as increasing
negativity at stimulus onset, occurred preferentially
for frequencies across the boundary between the
traditional delta and theta bands at 3–4 Hz, with
a smaller effect in the alpha band at 13 Hz. The
first of these effects is very large, with negative
driving occurring in 2y3 of the epochs. The oppo-
site effect in preferential phase occurrence was
apparent in the 6–9 Hz range, again spanning two
traditional bands (theta and alpha). This type of
phase reordering may be a new effect, as previous
196 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198
work has not explored preferential phase occur-
rence in relation to this variable. The absence of
negative driving effects at frequencies below 3 Hz
suggests that negative driving is not associated
with the CNV in these data.
The marked differences in occurrence of the
phases at stimulus onset, as a function of frequen-
cy, indicate substantial phase re-alignment, pre-
sumably associated with the fixed-ISI in this
paradigm. It needs to be considered in future work
how the frequency-dependent preferential occur-
rence of these phases develops over trials in a
fixed-ISI paradigm, and also whether it is apparent,
perhaps to a lesser degree, in paradigms with
varying ISI. The role of expectancy in these effects
is also of interest. Expectancy may be the con-
scious correlate of the preferential occurrence of
the brain states explored in this study, and it might
be useful to explore links between the cognitive
and physiological outcomes (particularly in rela-
tion to the CNV) of ISI manipulation.
An alternative interpretation, that these effects
merely reflect entraining of the EEG with the
fixed-ISI, appears unlikely. The stimulus onset
asynchrony here was 1372 ms, corresponding to a
frequency of 0.73 Hz. Such a frequency would be
substantially passed in the 1 Hz filter, and hence
simple entrainment might contribute to the mag-
nitude of the 1 Hz data streams, such as those
displayed in Fig. 4. But essentially no 0.73 Hz
activity would be passed by the other filters, and
hence entrainment frequency effects could not
underly the significant phase differences shown in
Figs. 5–7 which occur at frequencies above 1 Hz.
4.2. ERP component effects
4.2.1. N1
N1 amplitude is reduced for stimuli presented
during cortical negativity at 2–5 Hz; while
enhancement is apparent at 9–10 Hz. The first of
these effects is quite substantial, with N1 ampli-
tude reductions of approximately 40%. In contrast,
N1 amplitude is strongly enhanced by negative
driving for stimulus onsets at low frequency, par-
ticularly 1–3 Hz, but extending to 5 Hz. The size
of this effect is extremely large, with N1 amplitude
being amplified by a factor of 5 during negative
driving phases. There is also some reduction in
N1 amplitude for stimuli presented during negative
driving in the 7–9 Hz range. Together these
indicate that, with frequencies up to 5 Hz, N1
amplitude is strongly enhanced when stimuli are
presented in phases of negative driving and
reduced when stimuli are presented during phases
of cortical negativity. Weaker effects, but in the
opposite direction, occur with frequencies in the
alpha range. Such effects confirm the important
contribution to N1 by both slow wave and alpha
activity reported in previous work by Basar’s ¸
group (e.g. Stampfer and Basar,
¸ 1985), although
the delta contribution has not been as clear in
previous work. The actual enhancement of N1
with cortical negativity in the alpha band was
¸ and Stampfer (1985) and is also
noted by Basar
compatible with the early work on alpha-cycle
effects (e.g. Callaway and Yeager, 1960). The
weaker effect with negative driving in the alpha
frequencies is compatible with the findings of
Jansen and Brandt (1991) that N1 was enhanced
for stimuli presented when alpha was near a
positive-going zero crossing.
4.2.2. P2
The amplitude of P2 reflects cortical negativity
at stimulus onset strongly in the 1–3 Hz delta
range, beyond which there is no discernable impact
of this variable. In contrast, P2 amplitude is
reduced by negative driving at stimulus onset
strongly for delta activity from 1 to 2 Hz, and also
(but less strongly) in the 5–6 Hz theta range.
Together, these data (particularly the extremely
large delta effects, associated with )4-fold ampli-
fication) confirm the important contribution of the
delta and theta bands to the formation of P2, as
noted by Stampfer and Basar ¸ (1985). The impact
upon P2 amplitude of cortical negativity in the
delta range appears to be much stronger than
previously reported. However, there was no sup-
port here for Jansen and Brandt’s (1991) report
that P2 amplitude was affected by phase effects in
the alpha band. The concern was raised earlier
about their widening of the definition of alpha to
include activity between 5 and 20 Hz, and we
suggest that their wider frequency range may
underlie the discrepant results.
 R.J. Barry et al. / International Journal of Psychophysiology 47 (2003) 187–198
4.3. Functionality of preferred brain states
It is important to consider whether the differ-
ential occurrence of particular brain states found
here is functional, i.e. is a preferred brain state
associated with greater ERP component magni-
tude? For cortical negativity, the reduced occur-
rence of such states in the theta band, and their
greater occurrence in the alpha band, both contrib-
ute to enhanced N1, while their greater occurrence
in the delta band leads to enhanced P2. For cortical
negative driving, the preferential occurrence of
such states for frequencies across the deltaytheta
transition, and their reduced occurrence across the
thetayalpha transition, both enhance N1, and the
reduced occurrence of such states in the theta
range contributes to a larger P2. These data indi-
cate that the preferential occurrence of particular
brain states at stimulus onset does indeed contrib-
ute to optimising the brain activity reflected in
both the N1 and P2 ERP components. The chang-
ing profile of increased or decreased occurrence of
the states of cortical negativity and negative driv-
ing across the frequency range, and the different
relationships apparent for the two components,
indicates the complexity of this dynamic functional
process.
4.4. Conclusions
The results of the present study indicate the
preferential existence of particular brain states at
stimulus onset in a fixed-ISI auditory oddball
paradigm, and substantial differential effects of
these brain states on N1 and P2 amplitudes. These
data emphasize the importance of moving beyond
simplistic notions of the representative nature of
the average ERP. The differential effects of cortical
negativity and negative driving reported here rep-
resent a novel separation of phase effects into
independent factors. Previous research has con-
founded these factors and may have obscured both
the observation of any effects andyor their inter-
pretation. Overall, the finer-grained analysis of
frequency effects reported here clarifies the loci of
previously reported broad-band effects, and sug-
gests the value of future research in this vein.
Confirmation of these findings using alternative
197
methodologies, such as wavelet analysis, should
also be pursued.
The present data indicate important aspects of
brain dynamics, suggesting that in a fixed-ISI
paradigm the component frequencies of the EEG
are dynamically adjusted in order to provide par-
ticular brain states at stimulus occurrence to facil-
itate the brain’s processing of the stimulus.
Because of the need to obtain sufficient responses
for an adequate signal:noise ratio after partitioning
on the basis of phase at stimulus onset, the present
study was limited to an investigation of the
responses to background stimuli in the auditory
oddball paradigm. Nevertheless, the extremely
large magnitudes of the effects discussed above
clearly warrant further investigation. Studies are
needed to investigate these effects in the determi-
nation of ERP responses to both background and
target stimuli in an auditory oddball paradigm
modified to overcome this problem, as well as in
a wider range of paradigms.
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