Effects of tobacco smoking on topographic eeg and Stroop test in smoking deprived smokers

Prog. Neuro-Psychopharmacuf.

& Wol. Psych&. Copyright

2000, Vol. 24, pp. 535-546 0 2000 Elsevier Science

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EFFECTS OF TOBACCO SMOKING OR TOPOGRAPHIC EEG AND STROOP TEST IN SMOKIIUG DEPRIVED SMOKERS

XIAOJUAN XU1 AND EDWARD F. DOMINO’ ‘Department of Psychology, Grand Valley State University; *Department of Pharmacology, University of Michigan, Ann Arbor, MI, USA (Final form, April 2000)

Abstract Xu, Xiaojuan and Edward F. Domino: Effects of Tobacco Smoking on Topographic EEG and Stroop test in smoking deprived smokers. Prog. Nemo-Psychopharmacol. & Biol. Psychiat. 2000,24, pp. 535-546.02000 %evier Science Inc. 1.

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Quantitative electroencephalography (EEG) was used to measure human brain electrical changes produced by tobacco deprivation and smoking. Sixteen scalp cortical recording sites monitored regional changes in brain activity. The quantitative EEG was subdivided into delta, theta, alpha,, alph$, beta, and beta, bands for topographic mapping. A demanding version of the Stroop test was used to determine tobacco smoking effects on attention. The version used was more difficult than that used in previously reported studies. Healthy drug and substance free adult male and female volunteers were divided into nonsmoker (n=7) and smoker (n=7) groups according to their smoking status. They were instructed to abstain from tobacco products for at least 12 hr overnight before the next morning’s experiment. EEG was recorded before and after smoking either a fake placebo cigarette for nonsmokers or the cigarette of their choice for smokers. Subjects were also asked to perform the Stroop test before and after smoking the placebo or tobacco cigarette. The results showed that tobacco smoking significantly depressed delta and increased alpha, and beta, activity and slightly increased the Stroop effect. Although smoking one cigarette stimulated brain electrical activity of smoking deprived smokers, it did not improve performance on a difficult Stroop test.

Kevwords: attention, topographic EEG.

Stroop test, tobacco smoking, tobacco smoking abstinence,

Abbreviation: electroencephalogram

(EEG), electrocardiogram 535

(ECG)

536

X. Xu and E.F. Domino

Introduction Studies have shown that administration smokers

cause changes

of nicotine and nicotine deprivation

in the scalp recorded

electroencephalogram

noninvasive measure of changes in brain electrical activity. and Warburton, reported

1983; Pickworth

that 24 hr deprivation

(Comin,

et al., 1989; Knott, 1989). of nicotine

theta power.

in heavy

These effects

(EEG),

a

1980; Edwards

Ulett and Itil (1969)

smokers

decreased

frequency

and increased

cigarettes.

Knott and Venables (1977) found that 13 to 15 hr deprivation

in heavy smokers also decreased the alpha frequency.

in heavy

were reversed

alpha

by smoking of nicotine

Herning et al. (1983) showed

an increase in the theta power of heavy smokers after 4 hrs of deprivation.

Knott

(1988) and Golding (1988) reported

alpha

frequencies

that smokers showed a shift to higher

Thus, the results of several studies

after some form of nicotine intake.

suggest that short term nicotine deprivation

accompanies changing to slow activity in

EEG, and tobacco smoking increases brain wave frequencies. In the present study, the human EEG was further divided into six frequency delta (l-3.75

Hz), theta (4-7.5 Hz), alpha, (7.7510 Hz), and beta, (20.25-30

(12.75-20 frequencies

into one bandwidth.

Hz).

Hz), alpha, (10.25-12.5

Previous

studies grouped

bands:

Hz), beta, the alpha

Thus, it is possible that a decrease in the power of

lower alpha frequencies masked an increase in the power of higher alpha frequencies. One misses frequencies

important into broader

power

shifts

bandwidths.

within

the

A previous

alpha

bandwidth

by grouping

study employing

six frequency

bands showed that tobacco smoking shifted alpha EEG activity from alpha, to alp4 (Domino et al., 1992).

The present study employed six frequency

EEG was recorded

from

16 scalp positions to monitor regional changes in brain activity and topographic

EEG

precise changes in different frequency bands.

Furthermore,

bands to measure

mapping was used to characterize which regions of the brain show changes. Behavioral

studies have shown that tobacco smoking and nicotine

intake affect

human attention, the process that enables an individual to ignore the vast majority of information

and focus only on the relevant information.

One of the well established

paradigms

to study attention is the Stroop test (Battig,

1985; Battig, 1991; Estler,

1982).

In the Stroop test, a subject is required to identify the color of the inks in

Effects of tobacco smoking on which a series of color names are printed.

537

EEG and attention

The color names correspond

to the color Subjects

of the inks in which they are printed in some trials, but not in other trials.

find the incongruity of color names and the color of the inks in which they are printed The

very distracting and take longer to identify the color of the inks in such trials. performance

difference between processing conflicting information

Green printed in red letters) and processing nonconflicting

(such as the word

information

(such as the

word Green printed in green letters) is known as the Stroop effect, which reflects a failure of the attention process to ignore the irrelevant shown that nicotine improves

the performance

information.

Studies have

on the Stroop test and reduces the

Stroop effect (Wesnes and Warburton, 1978; Hasenfratz and Battig, 1992). whether nicotine improves question.

the attention process on a more difficult

The present study also investigated

attention by utilizing a computerized

the effects of tobacco

However,

task is still a smoking on

Stroop test, which is a more difficult

than those in existing studies. Furthermore,

version

the study explored any parallel effects of

tobacco use on the brain electrical activity and on the attention process.

Methods Subjects Healthy adult male and female subjects, ranging in age from 20-40 years, and free from any medication

or drug use, were recruited

through

advertisements.

Subjects

were divided into two groups according to their smoking status. One group (n=7, including 4 females and 3 males) consisted of nonsmokers who inhaled air through a sham cigarette during the experimental

session. The other group (n=7, including 4

females and 3 males) consisted of moderate to heavy tobacco smokers (l-2 packs/day). Subjects were instructed

to abstain from

drinking

any caffeinated

beverages

or

alcohol, using any medications or drugs, or any form of tobacco for the 12 hr period before the experiment

which was conducted in the morning.

On the morning

of the

experiment, subjects were questioned about their compliance with the no drinking, no drugs and no smoking requirement, and the informed consent was then obtained.

538

X. Xu and E.F. Domino

EEG and ECG Recording The experiment

utilized

16 cortical

recording

reference lead per the lo-20 International of Clinical Neurophysiology,

sites linked to A, and A, as the

System (Recommendations

1983). An electrode cap (Electrode

for the Practice Cap International,

Eaton, OH 45320) was placed on each subject’s head with Grass electrode gel applied to each electrode. The EEG recordings taken from F7, F,, T,, T,, T,, T,, FP,, FP,, F,, F,, C,, C,, P,, P,, 0,, electroencephalograph taken from recordings

and 0,

were

recorded

on channels

(Model 8-24D, Grass Instruments,

the right arm and left leg was recorded were transferred

1-16 of a Grass

Quincy, MA 02169). ECG on channel

to a Zenith 386/25 microcomputer

17. The EEG

directly

and were

analyzed by the computer software package RHYTHM 7.1 (Stellate Systems, Quebec, Canada). Color topographic

maps were printed by a Hewlett-Packard

Paintjet (Model

3630A, Hewlett-Packard

Co., Rolling Meadows, IL 60008). The EEG was analyzed in

each of six bandwidths:

l-3.75 Hz (delta), 4-7.5 Hz (theta), 7.75-10 Hz (alpha ,),

10.25-12.5 Hz (alpha ,), 12.75-20 Hz (beta ,), and 20.25-30 Hz (beta J. The Stroou Test The Stroop test used a Macintosh computer presenting nonconflicting information.

The information

was made up of six color words: red, brown, yellow,

green, blue, and purple; six colors corresponded of nonconflicting

information:

to the words. There were six types

red, brown, yellow, green, blue, and purple written in

red, brown, yellow, green, blue, and purple, respectively. conflicting

information:

60 trials,

and so on.

30 trials with nonconflicting

conflicting information.

There were 30 types of

the word red written in five colors except red, the word

brown written in five colors except brown, contained

or conflicting

One Stroop test session

information

and 30 trials with

The subjects were instructed by the computer to identify the

color and press key 1 for color red, 2 for brown, 3 for yellow, 4 for green, 5 for blue, and 6 for purple. Each key was labeled with a small piece of corresponding color paper.

In each trial, the computer presented either one color word written in

the color it indicated or written in other colors. When the subject responded, computer immediately time and accuracy.

the

presented the next trial. The computer recorded both reaction

Effects of tobacco

539

smoking on EEG and attention

Procedure The subjects were Macintosh computer

instructed

to follow

the instructions

on the screen

and practice the Stroop test after they arrived

area. After they finished practicing

the Stroop test, electrodes

of the

in the research

were affixed to the

skull and ears for EEG, right arm and left leg for ECG. Then they were instructed to relax in a reclined position and the light was switched off in the room. After two twominute practice perform

recordings

of eyes-closed

EEG and ECG, subjects were asked to

the Stroop test in a sitting position. When they finished the Stroop test,

subjects were told to close their eyes and relax in a reclined position. One two-minute session of eyes-closed

EEG was recorded.

Then the subjects were

minutes to smoke either a sham cigarette or a cigarette minute session of eyes-closed EEG was recorded subjects were then instructed to perform

allowed

five

of their choice. One two-

immediately

after smoking.

The

the Stroop test again. The Stroop test was

always performed with the lights on and the EEG was always recorded with the lights off. Statistical Analysis The differences

between EEG before smoking and after smoking were tested using

two-way ANOVAs with two within factors (2 conditions x 16 channels) on each of the six bands for each group. The differences between before and after smoking at each channel were tested using multiple mean comparisons

associated with the two-way

ANOVAs. The differences between the EEG of nonsmokers and smokers before smoking were tested using two-way

ANOVAs with one between factor and one within factor

groups x 16 channels) on each of the six bands. measures

(16 channels)

and one factor

(2

One-way MANOVAs with repeated

(2 groups)

were

also used to test the

differences between the two groups at each channel on each of the six bands.

Results The topographic maps of the mean EEG of nonsmokers before and after sham

After

I

05.56 81.13 76.69 72.25 67.81 63.38 58.94 54.58 58.06 45.63 41.19 36.75 32.3i 27.68 23.44 19.m

90.88 85.56 81.13 76.69 72.25 67.01 63.38 5B.94 54.58 50.9b 45.63 4L.19 X.75 32.31 27.88 23.44

Fig 1: Topographic EEG maps of nonsmokers and smokers. The top of the head is projected to a surface map with the nose above and the left hemisphere on the reader’s left, etc. Thus, the frontal cortex is above and the occipital cortex below. The upper series of colored maps shows the mean EEG before and after sham smoking in seven nonsmokers. The lower series shows the mean EEG before and after cigarette smoking in seven smokers, The colored calibrations represent voltage normalization for each frequency band.

SMOKERS

NONSMOKERS

Effects of tobacco smoking on EEG and attention

smoking show no significant change [Fig 1: upper panels].

541

However, the topographic

maps of the mean EEG of smokers before and after cigarette smoking show changes [Fig. 1: lower panels]. Two-way ANOVAs with repeated measure carried out on data for each band showed that tobacco smoking significantly decreased delta [F (1, 15) = 11.524, p < 0.011, and increased alpha, [F (1, 15) = 4.4931 and beta, activity [F (I, 1s) = 10.368, p < 0.011. activity

decreased

positions:

For the delta band, multiple comparisons

significantly

following

smoking

FP,, FP,, F,, F,, C,, C,, P, and P,.

comparisons

at the following

beta, activity increased

recording

For the alpha, band, multiple

showed that alpha, activity increased significantly

all sixteen recording positions.

showed that delta

following

smoking at

For the beta, band, multiple comparisons showed that

significantly

following

smoking at the following

recording

positions: T,, T,, FP,, FP,, F,, F,, C,, C,, P,, P,, 0, and Oz. A comparison

of the topographic

maps of the mean EEG of nonsmokers

before

sham smoking and the topographic maps of the mean EEG of smokers before smoking [Fig 1: left panel] suggested that tobacco deprivation decreased high frequency EEG activity.

increased low frequency

and

However, both ANOVAs and MANOVAs on

the mean EEG of nonsmokers before sham smoking and the mean EEG of smokers before smoking revealed no significant differences on each of the six bands. The results of the Stroop tests are shown in Fig 2. The upper two panels of Fig 2 show the mean reaction times and accuracy for nonconflicting

information

[Fig. 2:

upper panels], while the middle two panels show the mean reaction times and accuracy for conflicting information

[Fig. 2: middle panels]. Comparisons of the reaction times

indicate that the reaction times were shorter for nonconflicting for conflicting

information,

except the reaction

time of smokers

information

before smoking.

nonsmokers

made fewer mistakes for nonconflicting

conflicting

information.

for

and

conflicting

Comparisons of accuracy show that both smokers and information

between reaction

times to conflicting

and the Stroop effects measured by differences

conflicting

for

than those

than they did for

The lower two panels of Fig 2 show the Stroop effects

measured by differences information,

information

nonconflicting

information

[Fig.

and nonconflicting

between percent errors

2: lower

nonsmokers, the Stroop effects did not change after sham smoking.

panels].

For

For smokers, the

542

X. Xu and E.F. Domino

Times to NonconflictingInformations

Reaction

23

Nonsmokers Smokers

ReactionTimes to ConflictingInformation

Nonsmokers

Smokers

Accuracyfor NonconflictingInformation

Nonsmokers Smokers Accuracyfor Conflicting Information

Nonsmokers Smokers

600

c

g

500

;

400

5 k ;

200

8

100

R

300

0 -100

Nonsmokers Smokers Nonsmokers Smokers Groups Groups Fig 2: The upper four panels show the mean reaction times to and accuracy for Each bar in the reaction time panels nonconflicting and conflicting information. represents the mean reaction time f SE for 5-6 subjects, whereas each bar in the accuracy panels represents the mean percent errors f SE for 5-6 subjects. The lower two panels show the mean Stroop effects. Each bar in the left lower panel represents the Stroop effects measured by a difference between the reaction times to conflicting and nonconflicting information + SE for 5-6 subjects. Each bar in the right lower panel represents the Stroop effects measured by a difference between percent errors for conflicting and nonconflicting information & SE for 5-6 subjects. Stroop effects measured by differences

in reaction times slightly increased following

smoking, while the Stroop effects measured by differences in accuracy did not change following smoking.

However, the increase in the Stroop effects of smokers was not

543

Effects of tobacco smoking on EEG and attention

significant by a correlated t-test. The recording

of ECG indicated that sham smoking did not change heart rate of

nonsmokers whereas smoking significantly increased the heart rate of smokers [Fig 31.

lOO8060-

I

40-

l&p&e.

20O!

Nonsmokers

Smokers Groups

Fig 3: Heart rates of nonsmokers and smokers before and after smoking a sham cigarette or a cigarette. Each bar represents the mean heart rates per minute f SE for seven subjects. ** p < 0.01 Discussion Tonographic

EEG

The effects of tobacco smoking on EEG in the present study confirmed findings that tobacco smoking decreases low frequency

and increases high frequency

EEG activity (Knott, 1988; Golding, 1988; Domino et al., 1992). showed that tobacco

smoking significantly

the previous

decreased

The present study

delta activity,

alpha, and beta, activity in smoking deprived smokers.

but increased

Decreases in delta activity

occurred mainly in the frontal and parietal regions, while increases in beta, occurred mainly

in

Interestingly,

the

frontal,

parietal,

occipital,

and

the

right

increases in alpha, occurred in all recorded regions.

temporal

regions.

544

X. Xu and E.F. Domino

A comparison

of the topographic

maps of the mean EEG of nonsmokers

before

sham smoking and the topographic maps of the mean EEG of smokers before smoking suggested that smokers showed increased low frequency and decreased high frequency EEG activity following EEG of nonsmokers

tobacco deprivation,

although the differences

between the

and smokers before smoking were not statistically

significant.

Such differences in EEG may reflect the effects of nicotine withdrawal, suggesting the addictive nature of nicotine. reflect

individual

nonsmoker

It is also possible that such differences

differences

since subjects were not randomly

and smoker groups.

time will be able to address

in EEG may

assigned to the

Future studies focus on the EEG of smokers over the effects

of nicotine

withdrawal

Nonetheless, the present study suggested that tobacco deprivation

with certainty.

seemed to increase

low frequency and decrease high frequency EEG activity. Stroon Effects To make certain that the effects of tobacco smoking lasted throughout the Stroop test after smoking, recorded

another

two-minute

session of eyes-closed

following the Stroop test after smoking.

EEG and ECG were

Both EEG and ECG showed the

effects of tobacco smoking (data not shown). Thus, the Stroop test after smoking was carried out under the influences of tobacco smoking.

The results of the Stroop test

indicated that sham smoking did not affect the Stroop effects whereas tobacco smoking increased

the Stroop

effect

conflicting and nonconflicting

measured

by differences

information.

between

significant.

Comparisons

between

performances

smoking was not of

nonsmokers before smoking show that smokers responded to conflicting slightly faster than nonsmokers, nonconflict and conflict information smokers experience smokers identified names were printed.

times to

Because of great variations in the Stroop

effects among smokers, the increase in the Stroop effect following statistically

reaction

smokers

information

but they made slightly more mistakes for than nonsmokers.

and

both

Such results may suggest that

restless effects of nicotine withdrawal.

One nonsmoker

and two

color names instead of the color of the inks in which the color Their data were not included in the results of the Stroop test.

Their mistakes further suggested the difficulty of the version of the Stroop test in the present study. Thus, tobacco smoking did not seem to improve attention process on a

Effects of difficult

Stroop test, rather

tobacco

545

smoking on EEG and attention

the present study suggested an increase in the Stroop

effects. The recording of ECG suggested that sham smoking did not affect the heart rates but tobacco smoking significantly increased the heart rate (Fig 3). Thus, tobacco smoking produced stimulant effects.

Although tobacco smoking stimulated the brain electrical

activity and the heart beat, it did not seem to improve attention process required for a difficult task.

Conclusions 1. Smoking cigarette significantly decreased EEG delta activity, and increased alpha, and beta, activity in smoking deprived smokers. 2. Smoking cigarette did not seem to improve performance

of a difficult Stroop test.

3. Smoking cigarette significantly increased the heart rate.

Acknowledgments Supported in part by NIDA grants DA-07226, DA-10992, the Psychopharmacology Research Fund 361024, and Grand Valley State University grant-in-aid.

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Inquiries and reprint requests should be addressed to: Dr. Xiaojuan Xu Department of Psychology Grand Valley State University Allendale, MI 4940 1 USA E-mail: [email protected]