Scand. J . Psychol., 1974,15, 263-267

Effects of cigarette smoking on verbal rote learning and physiological arousal

KARIN ANDERSSON BIRGITTA POST

Abstract.-Verbal rote learning was studied on 12 moderate smokers. In one condition learning was inter- rupted twice by smoking a nicotine-containing cigarette (Virginia King, 2.1 mg nicotine) and in another condi- tion by smoking a nicotine-free cigarette. Immediately after the first nicotine-containing cigarette there was a drop in the number of correct responses and learning was significantly less rapid under subsequent trials as compared with learning after the first nicotine-free cigarette. After the second cigarette the picture was reversed. Learning was significantly more improved in the nicotine condition than in the nicotine-free condi- tion. Adrenalin excretion increased significantly during learning in both conditions, and heart rate increased sig- nificantly after the first nicotine-containing cigarette.

The present investigation is part of a research project concerned with behavioral and physiologi- cal reactions to cigarette smoking. In previous studies on dosage and time effects of smoking, Frankenhauser and her co-workers showed that adrenalin excretion increased progressively with the number of cigarettes smoked, and that the first cigarette produced the relatively largest changes in blood pressure, heart rate, skin temperature and hand steadiness (Frankenhaeuser, Myrsten, Was- zak, Neri & Post, 19681. These functions were also more affected b y strong cigarettes than by weak ones (Frankenhaeuser, Myrsten & Post, 1 970).

It has also been shown that cigarette smoking improves performance efficiency on visual reaction time tasks (Frankenhaeuser, Myrsten, Post & Jo- hansson, 197 1; Myrsten, Post, Frankenhaeuser & Johansson, 1971). Similar results have been re- ported by Heimstra, Bancroft, and DeKock (1967) in a study of simulated driving. Data from animal experiments show t t a t pretrial injections of nico- tine facilitate discrimination learning (Bovet-Nitti, 1969; Morrison & Stephenson, 1969), and that

The University of Stockholm, Sweden

post-trial injections improve maze-learning. The latter results have been interpreted in terms of the consolidation process, the assumption being that nicotine facilitates consolidation of the memory trace (Garg, 1969, 1970; Garg & Holland, 1967, 1%8).

The present study was designed to ascertain whether nicotine administered through cigarette smoking would induce changes in human learning. Verbal rote learning was studied in an experi- mental condition where the subjects smoked nico- tine-containing cigarettes and in a control condition where they smoked nicotine-free cigarettes. Cate- cholamine excretion and heart rate were also studied.

METHODS

Subjects, design, and procedure Twelve male university students participated in the ex- periments. Their ages ranged from 19 to 49 yr (mean 25.1) and their body weights from 60 to 85 kg (mean 70.3). They were all habitual smokers with a consump- tion not exceeding five cigarettes a day. Light smokers were chosen since they were assumed to be more sensitive to the low doses of nicotine administered.

Each subject attended one introductory session and two experimental sessions, where they smoked either two nicotine-containing cigarettes or two nicotine-free cigarettes. Possible positional effects were counter- balanced by rotating the Fequence of the two condi- tions. The interval between the experimental sessions was 5-7 days.

In the introductory session, held 2-3 days before the first experimental session, the subject learned two lists of seven nonsense syllables each, and smoked one-half cigarette of each kind. The heart rate equipment was demonstrated and information was given about factors that had to be under control in the night and morning before the experiments as, for instance, smoking, intake of coffee, drugs, or alcohol.

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264 I(. Andersson and 3. Post

The experimental sessions started at 8.30 a.m. or 9.45 a.m., and each subject had both his sessions at the same hour. After arriving in the laboratory the subject was served a light breakfast, and in a short interview it was ascertained that the instructions had been followed. After this a urine sample was collected and the test period, comprising 30 trials of verbal rote learning, was started. After trials 10 and 20 there was a break, during which the subject smoked one cigarette. Heart rate was recorded at fixed intervals throughout the session. After the last trial a urine sample was collected.

Cigarette smoking The standard cigarette used was of the brand Virginia King and contained 2.1 mg nicotine (according to cur- rent information from the Swedish Tobacco Cc-vpany). The nicotine-free cigarette was of the brand Br?o and made from the leaves of lettuce (Lactura Sativa, Texas, USA). Both were filter cigarettes and 80 mm long.

To counteract effects of expectation the subjects were told in advance that they would be given cigarettes containing nicotine in different doses. They did not know which kind of cigarette they smoked, the name of the brand being covered by a 10 mm piece of tape at the end of the filter. The tape also served as a mark for where the subjects were to stop smoking. The mean time for smoking one cigarette was about 7 min.

Verbal rote learning Two lists of nonsense syllables were used. Each list comprised 30 syllables, each consisting of a consonant, a vowel, and a consonant (e.g., buf, neb, etc). The syllables hadepreviously been rated by Swedish students as having a low association value (Bauer, personal com- munication).

The syllables were projected one at a time on a screen and the subject's task was to respond to each syllable by naming the next syllable in the sequence. The time of exposure was 3 sec and the inter-syllable interval was 1 sec. Each list was presented 30 times and the number of correct responses was counted for each trial.

Catecholamine excretion The subject was instructed to empty his bladder 1- 1.5 hr before the experiment started. Urine samples were collected by voluntary voiding before and after the learning period which lasted about 70 min. The urine volume was measured and pH adjusted to 3.5 with 2 N HCI. Specimens were stored at -18°C until anal- ysed by the fluorimetric technique of Euler & Lishajko ( 196 I ) .

Heart rate Heart rate was recorded by an electronic pulse meter (San-ei PM 101) using an ear electrode. Measurements were made during 30 sec at the beginning of the learning period, before and after each cigarette, and at the end of the session.

N i c o t i n e 0 N i c o t i n e - f r e e

0 6 12 18 2 L 30

Successive t r ia ls

Fig. 1. Mean number of correctly anticipated syllables on a verbal rote learning task in a nicotine and a nico- tine-free condition.

RESULTS

Verbal rote learning Fig. 1 gives a graphic presentation of performance in the learning task. A comparison between condi- tions shows that the pre-smoking scores nearly coincided. Immediately after the first cigarette there was a drop in the number of correct re- sponses in the nicotine condition and a tendency to less rapid learning was seen throughout the first post-smoking period as compared with learning in the nicotine-free condition. After the second ci- garette the curves of the two conditions followed almost the same course. The differences between the two conditions were analysed by calculating individual mean scores for pre-smoking (trial 1-10) and post-smoking periods (trial 11-20, trial 21-30). Post-smoking scores were then expressed as devia- tions from pre-smoking scores and values thus ob- tained were submitted to t-tests. It was shown that learning during the first post-smoking period in the nicotine condition was significantly inferior to learning in the nicotine-free condition (t= 2.32, d f = l l , p<0 .05) . There were no differences in learning between the two conditions during the second post-smoking period. In order to further analyse the effects of the second cigarette, scores from the second post-smoking period were ex- pressed as deviations from the first post-smoking period. t-tests showed that the gain in learning ability from the first to the second post-smoking

Scand. J . Psychol. 15

Effects of cigarette smoking on verbal rote learning 265

Table 1. Means and standard errors of adrenalin, noradrenalin and urine excretion in a nicotine-free and a nicotine condition

Nicotine-free Nicotine condition condition

Variable M S.E. M S.E.

Adr. excr., nglmin

Adr. excr., nglmin

Noradr. excr., ng/min

Noradr. excr., nglmin

Diuresis, ml/min

Diuresis, ml/min

presmo king 5.2 1 . 1 5.2 1 . 1

post-smoking 10.8 2.2 11.8 2.4

pre-smoking 20. I 1.5 23.3 1.5

post-smoking 21.3 2.4 22.6 2.6

pre-smoking 0.6 0.07 0.6 0.05

post-smoking 0.9 0.17 0.9 0.08

period was significantly more pronounced in the nicotine condition compared t o the nicotine-free condition (t=3.17, d f = l l,p<O.Ol).

Catecholamine excretion Means and standard errors for adrenalin, nor- adrenalin and urine excretion are shown in Table 1.

There was complete agreement between the two conditions with regard to adrenalin levels in the pre-smoking period. The values obtained after the learning period showed that adrenalin excretion increased significantly during both conditions ( t = 2.50 and 2.41, respectively, in nicotine and nico- tine-free conditions: df= 1 1, p<0.05). The fact that nicotine did not induce a further increase in adren- alin excretion is in agreement with previous results from experiments in our laboratory (Myrsten et al., 1971) which show that if the experimental situation is in itself stressful enough to increase adrenalin release, smoking does not induce a fur- ther increase.

There was no systematic change in noradrenalin output. Diuresis increased significantly (r=3.08 and 2.23 , respectively, in nicotine and nicotine- free conditions; df= I I . p<O.OS) during both ses- sions.

Heart rate Means for heart rate are given in Fig. 2 . The re- cordings made before smoking showed that heart rate was almost the same in both conditions. Im- mediately after the first cigarette, however, heart

0 N i c o t I ne- f ree c o nd'

0 2 L 6

Successtve m e a s u r e m e n t s

Fig . 2 . Mean heart rate at successive measurements in a nicotine and a nicotine-free condition.

rate was significantly higher in the nicotine condi- tion than in the nicotine-free condition (t=2.88, df= 11, p<0 .05) . Heart rate remained slightly more elevated throughout the nicotine session, but the differences between conditions did not reach statistical significance except a t the first post- smoking trial.

DISCUSSION

The results of the present investigation indicate that nicotine may have an initial detrimental effect o n the learning of nonsense syllables. The number of correct responses decreased significantly in the period following smoking the first nicotine-con- taining cigarette compared to the period following the nicotine-free cigarette. At the time for the second cigarette the picture was reversed. Learning was significantly more improved in the nicotine condition than in the nicotine-free condi- tion.

These findings may be explained in terms of a theory advanced by Walker (1958) relating per- severative consolidation. action decrement and arousal. The theory has its roots in the consolida- tion theory of memory originally proposed by Muller & Pilzecker (19001 according t o which each learning episode sets up an active, perseverative trace process in the central nervous system, which persists for a considerable period of time. Walker (1958) has extended the theory by stating that a temporary inhibition of recall occurs a t the same time as the fixating process operates o n the memory trace. High arousal during this period is assllmed to result in a more intense trace process,

Scand. 1. Psycho/. I5

266 K . Andersson and B. Post

leading to a better ultimate memory and to a greater temporary inhibition of recall.

Walker has produced evidence in favour of his theory in a series of experiments on behavior in the rat (Walker, 1956, 1958; Walker & Motoyooshi, 1%2; Walker & Paradise, 1958). The theory has also been supported by results obtained in two studies on paired associate learning in humans, showing that high arousal resulted in poor imme- diate recall but high recall after one week, while the opposite pattern was seen during low arousal (Kleinsmith & Kaplan, 1963, 1964). These re- sults have been replicated by Walker & Tarte (1%3).

The difference in recall in the nicotine and nicotine-free condition obtained in the present in- vestigation may be related to the level of arousal. The heart rate data show that arousal was higher after the first cigarette in the nicotine condition: a sharp rise in heart rate was recorded after the first nicotine-containing cigarette, while there was only a slight increase following the nicotine-free cigarette. The adrenalin excretion which also is assumed to reflect the level of arousal did not differ between conditions, however. A possible ex- planation to this might be that small transient changes are more difficult to observe by this tech- nique. In this context it should be mentioned that electroencephalographic studies show a rise in cortical activity a few minutes after smoking (Murphree, Pfeiffer & Price, 1967; Ulett & Itil, 1969; Philips, 1971). The fact that the second cigarette did not produce as pronounced changes in heart rate as did the first, is in line with previous results which show that the first cigarette is most potent in inducing psychophysiological changes (Frankenhaeuser et al., 1970).

Further investigations concerning the effects of nicotine on mental performance are planned, in which the results presented here will be followed up and examined further.

This investigation was supported by a grant from the Fund for Advancement of Graduate Studies, University of Stockholm, and by grants to Professor Marianne Frankenhaeuser from the Swedish Medical Council (Project No. 14X-997).

REFERENCES Bovet-Nitti, F. ( 1969). Facilitation of simultaneous

visual discrimination by nicotine in four “inbred” strains of mice. Psychopharmacologia 14, 193-199.

von Euler, U. S. & Lishajko, F. (1961). Improved tech- nique for the fluorimetric estimation of catechol- amines. Acta physiol. Scand. 51, 348-355.

Frankenhaeuser, M., Myrsten, A.-L. & Post, B. (1970). Psychophysiological reactions to cigarette smoking. Scand. J . Psychol. 11, 237-245.

Frankenhaeuser, M., Myrsten, A.-L., Post, B. & Jo- hansson, G. (1971). Behavioral and physiological ef- fects of cigarette smoking in a monotonous situation. Psychopharmacologia 22, 1-7.

Frankenhaeuser, M . , Myrsten, A.-L., Waszak, M., Neri, A. & Post, B. (1968). Dosage and time effects of cigarette smoking. Psychopharmacologia 13, 3 1 1-3 19.

Garg, M. (1969). The effect of nicotine on two different types of learning. Psychopharmacologia 15, 408- 414.

Garg, M. (1970). Combined effect of drug and drive on the consolidation process. Psychopharmacologia 19,

Garg, M. & Holland, H. C. (1967). Consolidation and maze learning: a comparison of several post-trial treatments. Life Sciences 6 , 1987-1997.

Garg, M. & Holland, H. C. (1968). Consolidation and maze learning: a further study of post-trial injections of a stimulant drug (nicotine). Znt. J. Neuropharma- col. 7 , 55-59.

Heimstra, N. W . , Bancroft, N. R. & DeKock, A. R. (1%7). Effects of smoking upon sustained per- formance in a simulated driving task. Ann. NY Acad. Sci. 142, 295-306.

Kleinsmith, L. J. & Kaplan, S. (1963). Paired associates learning as a function of arousal and interpolated interval. J . exp. psychol. 65, 190-193.

Kleinsrnith, L. J. & Kaplan, S. (1964). Interaction of arousal and recall interval in nonsense syllable paired associates learning. J . exp. psychol. 67, I24-126.

Morrison, C. & Stephenson, J. (1969). Nicotine injec- tions as the conditioned stimuli in discrimination learning. Psychopharmacologia 15, 35 1-360.

Myrsten, A.-L., Post, B., Frankenhaeuser, M. & Jo- hansson, G. (1971). Enhanced behavioral eficiency induced by cigarette smoking. [Rep. Psychol. Lab., Univer. Stockholm, No. 337.1

Murphree, H. B., Pfeiffer, C. C. & Price, L. M. (1967). Electroencephalographic changes in man following smoking. Ann. NYAcad. Sci. 142, 257-260.

Muller, G. E. & Pilzecker, A. (1900). ExperimenteUe B e i t ~ g e zur Lehre vom Gedachtnis. Z. Psychol. 1 , 1-288.

Philips, C . (1971). The EEG changes associated with smoking. Psychophysiology 8, 6474.

Ulett, J. A. & MI, T. M. (1969). Quantitative electro- encephalogram in smoking and smoking deprivation. Science 164, 969-970.

Walker, E. L. (1956). The duration and course of reac- tion decrement and the influence of reward. J . comp. physiol. psychol. 49, 167-176.

Walker, E. L. (1958). Action decrement and its relation to learning. Psychol. Rev. 65, 129-142.

Walker, E. L. & Motoyooshi, R. (1962). The effects of amount of reward and distribution of practice on ac-

172- 179.

Scand. J . Psychol. 15

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Effects of cigarette smoking on verbal rote learning 267

tive and inactive memory traces. J . romp. physiol.

Walker, E. L. & Paradise, N. (1958). A positive correla- tion between action decrement and learning. J . exp. psycho/. 56, 45-47.

Walker, E. L. & Tarte, R . (1963). Memory storage as a function of arousal and time with homogeneous and heterogeneous lists. 1. Verbal Learning and Verbal Behavior 2 . 113-1 19.

p ~ y ~ h o l . 55, 32-36.

Postal address:

Karin Andersson Psychological Laboratories University of Stockholm P.O. Box 6706 S-113 85 Stockholm Sweden

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