British Journal of Addiction (1992) 87, 1313-1326

RESEARCH REPORT

Cigarette smoking and cognitive performance GEORGE J. SPILICH,' LORRAINE JUNE^ & JUDITH RENNER^ ' Department of Psychology, Dunning Science Center, Washington College, Chestertown, MD 21620, USA, ^ Department of Psychology, Delaware State College, Dover, DE 19901, USA & ^ Allegheny County Law Department, 445 Fort Pitt Boulevard Suite 300, Pittsburgh, PA 15219, USA

Abstract While some investigations into the relationship between smoking and cognitive performance have reported that smoking facilitates performance, other research has come to the opposite conclusion. A review of the literature suggests that this variance in results may be due to differences among studies in design (comparing smokers only with deprived smokers rather than with non-smokers) and also to differences in task demands. Therefore, performance of smokers having just smoked, matched smokers deprived for a brief period, and also nonsmokers was contrasted on a series of tasks which ranged from repetitive and perceptually-bound tasks to complex, dynamic tasks dependent upon long-term memory. It was found that while cigarette smoking had no negative effect upon performance for simple perceptual tasks, smoking was found to exert measurable negative effects upon performance for more complex information processing tasks.

Cigarette smoking is a relatively common occurrence; in the United States alone, approximately 54 million adults smoke (Krasnegor, 1979). When asked why they smoke, one reason typically provided by smokers is that " . . . smoking helps me think and concentrate" (Wesnes & Warburton, 1983a). For example, Peeke & Peeke, (1984) have noted that smokers report an improvement in cognitive performance after smoking while Russell, Peto & Patel (1974) reported that 61% of their sample of heavy smokers felt that smoking facilitated their thinking and concentration. This perception of cognitive facilitation is supported by a considerable body of empirical evidence. For instance, Edwards et al. (1985); Frankenhaeuser era/. (1971)i Warburton et al. (1986); Wesnes & Warburton (1978, 1983b, 1984) and Wesnes, Warbur-

Requesls for reprints should be addressed to: George J, Spilich, PhD, Department of Psychology, Dunning Science Center, Washington College, Chesteno\vn, MD 21620, USA.

ton & Matz (1983) among others have reported that cigarette use improved the cognitive performance of active smokers over that of cigarette deprived smokers. Warburton and his colleagues rely upon this data to propose that cigarette smoking enhances cognitive performance due to changes in cholinergic mechanisms which affect encoding processes (Warbunon & Wesnes, 1984; Warburton et ai, 1986). Research which investigates drug effects upon cognitive processes must include a wide range of performance tasks which reflect in some fashion the complex and differentiated nature of cognitive processes (Weingartner, 1985). While the majority of the previously cited research has reported a facilitating effect of cigarette smoking upon performance, the target tasks typically employed in such studies are instructive: searching for periodicity in rapidly presented digit strings (Edwards et ai, 1985; Wesnes & Warburton, 1984; Wesnes & Revell, 1984); recognition of non-

1313

1314

George J. Spilich el al.

semantically encodable visual stimuli (Warburton et al., 1986), or a test of simple sustained vigilance (Mackworth, 1964) as Wesnes & Warburton (1978) and also Wesnes, Warburton & Matz (1983) have reported. Studies which rely on simple, rapidly-paced perceptually-based tasks typically conclude that cigarette smoking facilitates cognitive performance while other evidence (Andersson, 1975; Elgerot, 1976; Gonzales & Harris, 1980; Houston, Schneider & Jarvik, 1978; Kleinman, Vaughn & Christ, 1973; Stevens, 1976; Williams, 1980, for example) suggests that for tasks which depend heavily upon access to long-term memory or manipulation of information in short-term or working memory, nicotine may not facilitate and may even interfere with cognitive performance. A comprehensive review of the literature on smoking and cognition is available to the interested reader (USDHHS, 1988) while a review of methodological considerations for tobacco research is also readily available (Grunberg & Acri, 1991). How can we reconcile this variance in results and conclusions? In some studies, subjects smoked to obtain nicotine while in other studies, nicotine was administered via injection or tablet; in some studies, the performance of smokers having just smoked was contrasted only with deprived smokers while in other studies, the performance of smokers was contrasted with non-smokers; in some studies, the target task was simple and repetitive while in other studies, the task was complex. Different conclusions might therefore have resulted from differences in methodology. In an attempt to control for some of this variance while studying the effects of smoking upon cognitive performance, Ellinghaus (1983) contrasted the performance of three subject groups: non-smokers, smokers having just smoked, and those same smokers voluntarily abstaining from nicotine and caffeine for 3 hours prior to serving as a subject. Subjects were tested on three tasks: a simple visual search task delivered via computer, the Wechsler Memory Scale or WMS (Wechsler, 1945), and a text comprehension task involving the presentation and then free recall of two brief paragraphs. ElUnghaus reported that (a) non-smokers outperformed both smokers and deprived smokers, (b) deprived smokers showed a trend towards better performance than smokers, and (c) the performance advantage for the non-smokers over either active or deprived smokers was greatest for tasks requiring extensive LTM access (WMS, text comprehension) and less for the more automatic and

reaction-time bound task (a simple visual search task). To summarize, we know that cigarettes contain powerful psychopharmacological agents (Henningfield, 1984) and so it is reasonable to investigate their effect upon cognition. Evidence developed primarily from paced, perceptually-oriented tasks typically indicates that cigarettes are beneficial to mental performance; other evidence generated from tasks which emphasize manipulation of information in short-term memory (STM) and/or long-term memory (LTM) often comes to a different conclusion. The effect of cigarette smoking upon cognition, therefore, is not well established across a wide range of task demands. It was our prediction based upon the previously cited research that while smokers might have an advantage over non-smokers and deprived smokers in the performance of simple, paced, repetitive tasks with little or no demand upon LTM resources, a performance deficit would be observed when task demands increase in complexity and draw upon the contents of LTM along with the resources of working memory. In order to test this hypothesis, smoker's and nonsmoker's performance was contrasted on a series of tasks which extend along a continuum of processing complexity. That is, as the target task is more effortful, is less automatic, and relies more heavily upon access to episodic and semantic memory, we consider that the complexity of the task has increased (Weingartner, 1985). We make no claim that our battery of tasks is uniquely able to detect all the potential effects of nicotine or any other drug upon cognitive performance; only that a battery whose demands vary in complexity is better than a single perceptually-oriented task. Our goal was to observe the effects of cigarette smoking upon cognitive performance at a number of levels of processing analysis; a simple, visual, perceptual task with no substantive LTM involvement (Neisser visual search task), a visual attentional task where STM plays a small role in directing attention (VAT), a task considered to be an effective measure of STM operations (Sternberg task), a task requiring extensive use of LTM (text comprehension), and to bridge the gap between the laboratory and the real world, a simple computer-controlled driving simulator.

Method Subjecis Subjects in all five studies were college students; the majority were volunteers from an Introductory

Cigarettes and performance Psychology class. A total of 288 subjects served in these five experiments; 140 were male and 148 were female. Their mean age was 19.2 (SD = 1.2). Subjects grouped themselves as smokers or nonsmokers based upon a questionnaire which assessed smoking behavior. Non-smokers were defined as individuals who had never smoked regularly and who did not smoke now, whereas smokers were considered to be individuals who claimed to have smoked at least one pack of cigarettes per day over the last year. Smokers of cigars and pipes were excluded and an effort was made to exclude students who smoked anything else. While pre-experimental differences in SES, IQ, personality, and other variables might differentiate our smoking and nonsmoking subjects, it was deemed unethical to create comparison groups by requiring non-smokers to smoke or unreasonable to expect habitual smokers to suddently and completely abstain. Data collected from subjects who reported taking medication for colds or any other serious illness were not included in any experiment.

Procedure The same basic procedure was used for all experiments unless otherwise noted. Subjects were tested individually and after giving informed consent. There were a total of three experimental groups in each experiment: smokers who had just actively smoked (AS), smokers who were deprived (DS), and non-smokers (NS). No subject participated in more than one study. Smokers were alternately assigned to either the AS or DS conditions. The rationale for the deprived smokers condition was to assess the residual effect of chronic cigarette use and consequent low levels of blood nicotine and COHb along with the effects of nicotine withdrawal. In that sense, performance by the AS group demonstrated the acute effects of cigarette smoking. Smokers participating in the active smoking condition (AS) were provided with a cigarette containing 1.2 mg/cig nicotine (FTC Report, 1988). Each subject was requested to inhale normally every 25 seconds and hold that puff for 5 seconds, for a total of 12 puffs. The smoking procedure occurred in a waiting room where a large clock with a sweep second hand was prominently displayed; the experimenter was present during the smoking procedure to insure compliance. Deprived smokers were requested to abstain from smoking for 3 hours prior to serving in the experiment; all subjects indicated that they had complied. Subjects in all three groups were re-

1315

quested to abstain from coffee, tea, or soft drinks for a 2-hour deprivation period prior to serving in the experiment. Both the deprived smokers (DS) and the non-smokers (NS) also sat in a waiting room for the same 6 minute interval as the smoking subjects; they 'sham-smoked' an imaginary cigarette using the same procedure as the AS subjects.

Task 1: Neisser visual search task Neisser (1963,1964) was interested in the rapid and automatic processes of visual pattern recognition which occur during reading. He attempted to study the processes involved in analyzing the individual features of a target (such as the letter 'Q') embedded in a background (such as an array of letters). In this first study, each subject searched rapidly for a target letter embedded within a typed array of letters. A detailed description of the task is available in Massaro (1989).

Subjects A total of 45 subjects served in this experiment. The subjects were equally divided into NS, DS, and AS groups.

Procedure The Neisser visual search task was presented by a microcomputer equipped with ms timing capabilities. Each trial required a subject to visually search a 96 letter search array (12 rows by 8 columns) for the occurrence of a target letter. Both targets and arrays were capital letters. In half the trials, the target and the array were both similar (i.e. the angular target letter 'X' was placed somewhere in an array of angular letters such as K, T, V, W, or a rounded target letter 'O' placed somewhere in an array of rounded letters such as Q, U, C, D). In the remaining trials, the target/array relationship was dissimilar (i.e. a rounded target in an angular array or an angular target m a rounded array). Each of the four possible conditions (target angular, array angular; target angular, array rounded; target rounded, array angular; target rounded, array rounded) occurred equally often for each subject. At the beginning of each trial, a general set of instructions was provided for each subject to read aloud to the experimenter. Several practice trials then ensued; subjects were offered further practice but no subject requested this additional practice. After becoming familiar with the task, each subject

1316

George J. Spilich et al.

participated in 48 trials. Each trial consisted of the presentation of a target letter (i.e. 'X' or 'O') and then the presentation of the search array; subjects searched the array as quickly as possible from top left to bottom right and pressed the space bar as soon as they had located the target in the array. In order to validate the accuracy of each subject's selfreport of target location, the slope of the function relating RT to number of items searched was computed for the three groups. It was assumed that a linearly increasing function relating number of items searched to decision RT indicated that the group was following instructions; such functions were observed for all three groups. A microcomputer recorded the search time for each trial; no feedback regarding performance was provided.

Results The results are presented in Fig. 1. Analysis of variance showed that there was no significant difference among the three groups when performance was collapsed across all target/array conditions, F < 1 . However, in line with what Neisser (1963) has reported, search time for all three groups was reliably quicker for those trials presented in the target/array dissimilarity condition than for trials in the target/array similarity condition, F ( l , 4 2 ) = 113.6; ^XO.OOI. The interaction between group and target/array congruence was not significant, F < 1.

10-] "

9-

^

7-\

I Similar Dissimilar Target/array congruence

Figure 1. Median search time as a function of group and target-background congruence.

Summary

On a task which requires low LTM access, is high in automaticity and places no appreciable demands on long-term memory, we see no statistically reliable change in performance attributable to cigarette smoking.

Task 2: Visual/Attentional task The Visual/Attentional task, or VAT, requires a subject to detect a change in one member of a set of visually presented items. To perform this task, one must search the screen continuously until the change is detected.

Subjects The criteria for differentiating smokers from nonsmokers described previously was applied again to yield a total of 60 undergraduate subjects divided equally into AS, DS and NS groups.

Apparatus Materials were administered using a microcomputer equipped with ms timing capabilities. Each trial in the Visual/Attentional task (or VAT) consisted of the following. Subjects initiated each trial by pressing the space bar. After a short pause, a CRT screen filled with a search set of 20 identical letters. In a third of the trials, all 20 letters in the search set were the letter 'B'; equally often the search items were all 'O's or all 'M's. After an anticipation interval one of the letters in the search set would turn into a target letter; this transformation was instantaneous from the subject's perspective. In the case of the 'B' screens, a single 'B' in the search array would turn into a target 'E'; for the 'O' screens, one 'O' would transform to a 'Q' and for 'M' screens, one 'M' would transform into an 'N'. The subject's task was to respond by pressing the space bar as soon as the transformation of a single search item into a target letter had occurredSubjects were not informed of the duration of the anticipation interval; in fact, over the 24 trials, anticipation intervals of 5, 10, 15, and 20 seconds were equally distributed. These four anticipation intervals were counterbalanced across each of the three target (B, O, and M) screens. Anticipation errors or trials where subjects indicated that the target had appeared when in fact it had not were handled by having the computer alert the subject as to their error and then adding the missed trial to the

Cigarettes and performance

1317

set of trials yet to come and then reordering those trials. No group differences in anticipation errors were observed; in fact, such errors were infrequent. The VAT is conceptually similar to a task employed by Vurpillot (1968) to study the development of attentiona! capacity in children.

Procedure At the start of the session, subjects read aloud a brief explanation of the experimental procedure and were made to understand that their task was to scan the search array and, as quickly and accurately as possible, press the space bar when they noticed the search item/target transformation. A set of practice trials came next to insure that the subject was both warmed up and familiar with the task. When the subject was ready, the experiment began. The experimental procedure consisted of a total of 48 valid trials; subjects progressed to a new trial by pressing the space bar.

Results Median reaction times for the NS, DS and AS groups were 2.13, 2.81 and 2.52 seconds, respectively. Analysis of variance indicated that there were significant differences in group performance, F(2, 57) = 6.04 p < 0 . 0 1 . Bonferroni r-tests for preplanned comparisons (Kirk, 1968) showed that the NS group was significantly quicker in observing the transformation than either smoking group, and the active smoking group reacted to the transformation reliably faster than did the deprived smokers. No other main effect such as delay interval (5, 10, 15, 20 seconds), transformation (B-E, O-Q, or M-N), or any interaction between group and other main effect was significant. These results are presented graphically in Fig. 2.

Summary The Visual/attentional task has a very slight LTM component in that a subject typically optimizes their performance by maintaining a regular search pattern through the display. In this task, the performance of the non-smokers was superior to that of either smoker's group, while smokers who had just smoked were found to have outperformed the deprived smokers on this simple task which is highly perceptual and dependent upon automatic visual processes.

NS DS AS

10 15 Deloy ot transformotion (sec)

20

Figure 2. Response latency as a function of group and delay of transformation.

Task 3: Sternberg task Sternberg (1969, 1975) has described an elegant procedure which allows us to examine the subprocesses of search through the contents of short-term memory. In the typical Sternberg task, a subject is visually presented with a sub-span list of items such as letters or numbers. This list known as the search set. After a brief presentation interval, a test item is presented to the subject; the subject then quickly and accurately decides if the test item was a member of the search set. Performance on a Sternberg task is generally interpreted in terms of rate of search through the contents of STM, and also a separate factor related to encoding processes and neural transmission times. As Smith & Langolf (1981) have reported that factory worker's Sternberg performance was affected by chemical exposure, it might reasonably be expected that this task would be useful in the present setting. Further discussion of the implications of this task are widely available (see Crowder, 1976 and also Massaro, 1989).

Subjects A total of 63 subjects participated in this study, equally divided into NS, AS, and DS groups.

Procedure Subjects were tested individually. They were seated before a microcomputer with ms timing capabilities; the index finger of their dominant hand resting on one key to signal 'Yes' while the corresponding finger of their other hand rested on another key symmetrically situated to signal 'No'. Subjects were

1318

George J. Spilich et al.

Analysis of the number of errors (that is, responding 'Y' when the probe item was not present on that trial, or 'N' when it was) revealed the following results. The mean percentage of errors committed by the NS, DS, and AS groups was 6.8, 11.5, and 15.6, respectively. This difference was significant, F(2, 60) = 4.78,;> < 0.05. Bonferroni ttests revealed that the non-smoking group made significantly fewer errors than either smoking group, and also that deprived smokers made significantly fewer errors than active smokers. Lastly, the regression line for each subject's data was computed and two simple ANOVAs were performed using the slope and the Y-intercept of the performance function for each subject as raw data. Once again, the slope of the Sternberg function is considered to be a 'pure' index of time to manipulate and compare information in STM, while the Y-intercept is considered to be a measure of other factors related to general speed of processing (Lachman, Lachmand & Butterfield, 1979). Mean slopes for the NS, DS, and AS groups were 72.1, 81.3, and 91.2 ms, Results Analysis of variance revealed the existence of a respectively. There was a significant difference significant performance difference among the among the slopes for the three groups, groups, F(2, 60) == 7.27, jXO.Ol along with the F(2,60) = 8.43,/XO.Ol. Pre-planned comparisons expected longer search time for larger search sets, among the three groups indicated that the nonF(5, 300) = 76.05, p < 0.001. Bonferroni Mests smokers searched the contents of the search set revealed that the NS group searched STM reliably significantly faster than either smoking group, and quicker than either the active or deprived smoking that scanning was slightly but reliably faster for groups. However, the trend towards a performance deprived smokers than for those who had just advantage on the part of the deprived smokers over smoked. the active smokers was not statistically reliable. A similar analysis on the Y-intercepts of the three Figure 3 presents time to search through the functions was performed. Mean Y-intercepts for the memory set for the three subject groups. NS, DS and AS groups were 626.6, 933.9 and 995,7

requested to respond quickly but accurately. After the experimenter provided a brief verbal description regarding the nature of the task, the program presented a series of practice trials. Both practice and experimental trials consisted of the presentation of a search set which varied between one and six items. Items in the search set were single digit numbers and were presented individually at the rate of one item per second. A plus ( + ) sign signaled the end of the list, and then the probe item appeared. Subjects responded either 'Y' or 'N' via the keyboard after deciding as quickly and accurately as possible whether or not the probe item had appeared as a member of the search set. A total of 84 experimental trials was presented to each subject. Output from the procedure consisted of both decision times in ms for search sets of various sizes and also error rates for decisions.

ms, respectively; this difference was significant, F(2, 60) = 5.14, p < 0 . 0 1 . Pre-planned comparisons support what the eye suggests from inspection of Fig. 3; non-smokers were significantly faster than smokers in processes reflected by the Y-intercept but no reliable differences separated the active and deprived smoking groups.

1600

600 3 4 Sizeofseorchset

5

Figure 3. Median RT to respond as a Junction of group and size of search set.

Summary This study suggests that smoking exerts a measurable and negative effect upon the data manipulative operations of STM; furthermore, that this negative effect persists among smokers during at least the initial period of smoking deprivation. One of the residual effects of smoking appears to be an increase in non-comparison STM processes, as is evidenced by the significant difference in Y-intercept between the non-smokers and the two smokers groups;

Cigarettes and performance

1319

comparison time in STM appears to show both residual and acute effects, as demonstrated by the differences in slope among the three groups. Smokers also generate more errors on this task than do non-smokers. These conclusions contradict the results of West & Hack (1991), who report that scanning the contents of STM is quicker after smoking a nicotine cigarette than after smoking a non-nicotine cigarette, However, West & Hack (1991) used a very different procedure than that employed in the present study. West ei at. used only active smokers as subjects and collected data on search set sizes 2 and 5 only. These differences in procedure may explain the variance in conclusions; further work is needed to clarify this disparity in results.

hension of text is analogous to the demands of everyday problem-solving: we must use our previous knowledge and experience to make sense and structure out of a confusing and ambiguous array of information. A well-developed methodology exists to decompose text into atomistic idea units known as propositions; these propositions can be related in terms of the degree of their relatedness to the central theme of the passage. Numerous sources exist which discuss theoretical and pragmatic aspects of text comprehension; see, for instance Flammer & Kintsch, 1982; Kintsch & van Dijk, 1978; Lesgold & Perfetti, 1981; Spilich, 1985; Vipond, 1980; and Voss, Tyler & Bisanz, 1982.

In experiments 1 to 3, the tasks involved were tasks which could be described as primarily 'frontend' tasks. That is, successful performance of these tasks requires little in the way of access to semantic memory and also little in the way of conscious, guided effort through the use of working memory. The Neisser search task is considered to be a primarily front-end or feature detection task; the Visual/Attentional Task is perceptual but requires a slight amount of LTM resource in order to track the array in a strategic fashion. The Sternberg task is assumed to require additional resources to manipulate data in the working memory buffer. A case could be made that as we progress from Neisser through Visual-Attentional to Sternberg tasks, we are progressing along a dimension which was primarily perceptual processing and minimal reliance upon LTM at one end-point and a greater reliance upon LTM and complex processing skills at the other end-point. Earlier, we had proposed that cigarettes might begin to exert measurable effects upon cognitive operations as task demands increase. Therefore, the residual and acute effects of smoking were assessed by tasks which rely heavily upon one's ability to successfully deploy the contents of LTM.

Subjects A total of 60 subjects selected from the Introductory Psychology pool participated in this study; they were equally divided into NS, AS, and DS groups.

Task 4: Discourse comprehension In order to comprehend text, one must engage in a number of tasks: featural analysis of the stimulus set, access to both phonological and orthographic information as an aid to decoding words from the stimulus array, access to the internal lexicon in an effort to represent the meaning of each word, and access to contextual information (both grammatical and linguistic) as an aid to decoding the semantic structure of each sentence. In many ways, compre-

Materials The story employed was a passage entitled 'William Kemmler: A true electrical pioneer'. It described the historical events surrounding the first execution through electrocution. The story has two interwoven plots; one relates the circumstances leading up to the execution of the hapless Mr Kemmler while the secondary plot details the struggle between Thomas Edison and George Westinghouse over the advantages of direct current (DC) over alternating current (AC); Mr Kemmler's execution played a pivotal role in this controversy. Subjects spontaneously reported that the story held their interest; it was hoped that an intrinsically interesting story would lead to sustained effort on the part of the subject.

Procedure Each subject was tested individually. Subjects were told that they would be asked to read a story aloud and that they would later be asked to recall that story. Recall instructions stressed both accuracy and completeness; subjects were informed that while no one could be expected to recall the story in its entirety or without error, they should try to recall as much as they could as accurately as possible. They were also instructed that if they could not recall information exactly as it was presented in the story, they should try to come as close as possible by choosing words and phrases which capture the

1320

George J. Spilich et al.

underlying meaning. Such instructions have been shown in the past to produce reasonable represemations of what was actually comprehended by the reader (Kintsch et al, 1978; Spilich et ai, 1979). Each subject orally free recalled the story; the resultant protocols were tape recorded and subsequently propositionalized according to the guidelines presented by Turner & Greene (1977). Two raters blind to group status independently scored a random sample of five protocols from each group; the inter-rater correlation coefficient was 0.91.

Results Figure 4 illustrates the recall of propositions by group and by importance to the theme of the story, where level 1 propositions are classified as thematically central ideas and level 4 + propositions are considered to be relatively unimportant details. The recall function presented by the non-smoking group is quite similar to recall functions reported elsewhere (Dixon et al, 1982; Kintsch et al, 1978; Miller & Kintsch, 1980; Spilich, 1983, 1985; Spilich et al, 1979; Vipond, 1980) for college students reading other texts, and so the present procedure appears valid. Analysis of variance using the dependent variable of propositions recalled as a function of group and thematic level showed the following. There was a significant difference in free recall of textual material among the three groups overall; F(2, 60) = 22.4, p < 0 . 0 1 . Bonferroni r-tests showed that the non-smokers recalled significantly more information than either smoking group, and also that deprived smokers recalled more information than did their counterparts who had smoked just prior to the text comprehension task. More theoretically interesting was the change over the three groups in the slope of the function relating recall to thematic level. The performance of the non-smoking group in the present study was similar both quantitatively and qualitatively to results presented by other researchers using other stories, subject pools and procedures (Spilich ei al, 1979; Kintsch et al, 1978). The typical explanation attached to the function described here is that subjects are using previous knowledge to selectively attend to central idea units rather than relatively trivial details, and so the 'falling' function described by the NS group reflects this structuring of processing deployment. The recall functions described by the DS and then AS groups appear respectively to turn increasingly 'fiat', that is, to reflect less and less a selective deployment of

—D— NS —A— DS . . • • • • • AS

40-• \

30, -

1

2

3

^

4

Thematic level

Figure 4. Percentage of propositions recalled as a function of group and thematic level

attention to critical items within the text. These data suggest that smoking cigarettes in general is linked not merely to poorer recall but to a decreased ability to differentiate critical items from items of lesser importance; furthermore, this effect exists not only for the acute effects of smoking (AS subjects) but even for the residual effects of cigarette smoking (DS subjects). In an effort to quantify this apparent flattening of selectivity of processing, a regression line was calculated for each subject's recall and the resultant slope for each subject's thematic recall function was used as raw data for an ANOVA among the groups. Mean slope for the NS, DS and AS groups was —7.4, —2.9, and —0.7 propositions, respectively. It was found that a significant difference existed among the groups, F(2, 60) = 16.52, p < 0.01; Bonferroni (-tests showed that the slopes of all three groups significantly differed one from another.

Summary Cigarette smoking was related to decreased performance on a text comprehension task possibly by diminishing the ability of the smoker to deploy processing operations selectively to capture those events which were central to the task.

Task 5: Driving simulation Diehl (1969) has indicated that smokers are disproportionately represented among vehicular and industrial accident victims. DiFranza et al (1986) have reported that, for a 1 year sample, the ratio of

Cigarettes and performance smoker's to non-smoker's vehicular accidents was 1.46:1.00 even when differences in alcohol consumption, age, driving experience, and education were considered. Similar results suggesting that smokers are more likely to be involved in vehicular accidents have been reported by Adams & Williams (1966) for male insurance applicants, McGuire (1972) for male Air Force recruits, and by Waller (1986) for fatal accidents. While disentangling the effects of cigarette smoking from concomitant variables such as alcohol use is not easy, these studies indicate that cigarettes may play a causal role in vehicular accident patterns. This role might be twofold: accidents caused by the act of smoking and accidents caused by the effect of smoking. It was our intention to differentiate accidents due to the smoking procedure (inattention due to ash falling on clothing or fumbling for matches) from changes in cognitive operations brought about by smoking itself; our subjects were therefore asked to smoke just prior to serving as a subject but were not allowed to smoke while driving the simulator. In order to test the effects of cigarette smoking upon driving performance in a controlled environment, a driving simulator was employed. As driving even a simple simulator places demands upon a variety of processing operations (visual analysis, attention, LTM, problem-solving) it was hoped that such a task would reflect real-world performance, albeit imperfectly.

Subjects A total of 60 subjects participated in this study; they were equally divided into NS, AS, and DS groups as described previously.

l^ocedure Subjects were tested individually; the procedures for smoking were identical to those previously described. Subjects were seated in front of a computer-driven driving simulator. A steering wheel, gear shift with two forward gears and a foot operated gas pedal were under the driver's control. A color monitor whose screen was 63.5 cm on the diagonal was positioned 0.914 m from the subject at eye-level. The computer presented each subject with a road race wherein the object was to stay on the road and avoid accidents as long as possible. The road twisted and turned; obstacles such as oil slicks and other competing cars would unexpectedly present themselves. Each subject was given a 5 min

1321

warm-up period to learn about the game; no subject requested additional time when it was offered. Subjects were asked to estimate the average period of time they spend weekly playing video games; these estimates varied greatly within groups and there was no reliable difference in such estimates among the three groups. Two dependent variables were used: length of game and number of rear-end collisions; each collision cost time and so adversely affected one's performance. Subjects were instructed to stay in the game as long as possible by maintaining a quick pace and avoiding accidents.

Results Mean session duration by the NS, DS and AS groups was 3.5 min, 3.6 min, and 4.3 min. This difference was not significant, although pre-planned comparisons indicated that the additional time played by the AS group when compared with the pooled NS and DS groups suggested a slight trend in that direction. There was a significant difference in collisions among the three groups F(2, 57) = 16.19, p < 0.001. Bonferroni t comparisons showed that the difference between the NS and DS groups was not significant, but the difference between the active smokers and both deprived smokers and nonsmokers was significant. That is, those individuals having just smoked were involved in significantly more rear-end collisions than either the nonsmoking or the smoking deprived individuals. Analysis of covariance with length of time played as a covariate showed that the additional time spent at the wheel by the active smokers was not a significant contributing factor to the AS group's unusual performance. Figure 5 shows rear-end collisions for the three groups expressed both in terms of absolute number of collisions and in terms of collisions per unit time.

Summary In light of the previously described research reporting that smokers are disproportionately involved in vehicular accidents (especially rear-end collisions), it seems noteworthy that in a controlled study involving a computer-driven driving simulator wherein subjects were instructed to drive for as long as possible without accident, smokers who had just smoked were involved in almost 3.5 times as many rear-end collisions as the non-smoking group.

1322

George J. Spilich et al. 12

10• 2

—

6-

cr

sources and working memory. Visual inspection of Figure 6 suggests strongly that for rapid, perceptually-based tasks such as the Neisser, no difference among the three groups was observed but as the task comes to rely more heavily upon working memory and LTM access, the performance of smokers in general and active smokers in particular declines when compared with the performance of nonsmokers.

4-

• Collisions - D - - Coll/Minute NS

DS

AS

Driving

Group

Figure 5. Rear-end collisions by group.

Discussion At the start of this paper, we proposed to investigate the effects of cigarette smoking upon performance for a variety of cognitive tasks. Our tasks ranged from tracking a single target to tracking multiple targets; from automatic to consciously guided processes; from simple perceptual processing to processing which is heavily dependent upon access to semantic and episodic memory. It was proposed that as we moved from task to task along a dimension wherein access to LTM and working memory load increased, a deficit associated with smoking would appear. In order to compare all the experiments collectively, the ordinal rankings of performance were collected for all three subject groups across all tasks. Ordinal rankings were used instead of percentage improvement ratings or ^-scores, because we felt such a contrast would be less misleading than to compare directly a 10% or 1 SD measure of performance between two tasks where the dependent variables are as different as time to locate a visual target and recall of idea units in text. Clearly, recalling 10% more of the most important idea units in a story is not comparable in information processing terms to showing a 10% improvement in reaction time to a simple stimulus. Figure 6 presents the relative rankings of the three subject groups across all five tasks, where a ranking of T indicates the group with the best performance on that task, and a '3' indicates the group with the worst performance on that task; non-significant differences are treated as tied ranks. The axis from the Neisser task through to the driving simulation task roughly represents a gradient from highly automatic and perceptual processing towards greater demand upon problem-solving skills and upon LTM re-

1 2 Relative performance Figure 6. Relative performance rank by groups for each experimental task (ID, smokers; Q, deprived smokers; M, non-smokers).

In light of the previously summarized body of research investigating nicotine's effects on information processing, we interpret the present data to indicate that sub-processes such as working memory or attentional capacity which are involved in dealing with complex tasks are disrupted by an agent or agents in cigarettes, with nicotine itself and/or carboxyhemoglobin our prime suspects. Our work has several implications. The most important might be that a cognitive performance deficit due to smoking would be covert until task demands exceed the individual's capacity. For example, the effects of smoking upon driving performance might not appear to the skilled adult driver unless a tyre were to suddenly fail; then the increase in task demands when pressed against a lowered upper limit of capability could have negative consequences. Similarly, an airline pilot might experience a meaningful deficit in judgement after smoking if a situation arose wherein all of his or her judgement and experience were needed in an emergency. Our data indicate that it is exactly at the point of heavy task demands and complex problem-

Cigarettes and performance solving that the performance deficit linked to smoking would be maximized. Another obvious conclusion is that chronic smoking may exacerbate already existent memory problems. It has been reported that changes in regional cerebral blood flow (rCBF) accompany chronic smoking (Yamashita et ai^ 1988). We already known that regular changes in rCBF accompany intellectual changes among the elderly (Knezevic et al., 1989; Mubrin e: a/., 1989), and it has been reported that cerebrovascular changes are linked to memory problems in chronic smokers recovering from ischemic heart disease (Frasure-Smith & Rolicz-Woloszyk, 1982). Subtle but important changes m rCBF brought about by smokmg may explain Hill's observation (1989) that chronic cigarette smoking negatively affects elderly individual's performance on speeded mental tasks. We hope in future work to gain a clearer picture of the possible role which rCBF, carboxyhemoglobin and aging may have in modulating the effects of nicotine upon cognitive operations. Interestingly enough, earlier work which claimed that nicotine improved cognitive performance has lead some to suggest that nicotine be used as a cholinergic agent in the treatment of Alzheimer's Disease (Newhouse el al, 1988). Such conclusions may be premature, if based upon investigations employing only simple perceptual tasks. In addition to the acute effects of smoking which are indexed by comparisons between the NS and AS groups, the comparison between the active and deprived smokers indicates that deprivation may also exert an effect upon cognitive performance. That cigarette deprivation may adversely affect performance among smokers is not a novel idea (Heimstra, Bancroft & DeKoch, 1967; Kleinman et al, 1973) but the present data expands upon this notion to indicate that deprivation effects upon mental performance are also a function of task demands. Although the present work dealt entirely with active smokers, it is only natural in light of these results to speculate regarding the effect of passive smoking upon one's cognitive performance. Bauman, Koch & Fisher (1989) examined the effects of smoking by household members upon the California Achievement Test (CAT) performance of nonsmoking children living in a smoking household. Their results are summarized in Figure 7. As smoking among household members increased from 0 to > 2 packs/day, CAT performance declined even when mediating factors as age, sex, race, parental education, and personality variables were

1323

covaried. Regardless of whether smoking exerted its effects pre- or post-natally, this putative relationship between parental smoking and cognitive performance by non-smoking children is intriguing. How passive smoking might affect performance on a battery of tasks like our own is not yet clear.

—C^ CAT Total - - # — Moth

[; ^

630-

•••"

1• O N •

1 620j

c 1

^"*"«'

— - Q - - Spelling

" " • • • - \

1

3 610600-

590None

1cig-1 pack

>2pk

Group

Figure 7. Familial smoking and CA T scores for adolescent non-smokers, controlling for selected background variables (Bauman et al., 1989).

In future work, we hope to expand our interests in the effects of smoking upon performance to include designs and tasks which would specifically focus upon gender differences in performance. Gninberg, Winders & Wewers(1991) have provided a comprehensive summary of the issues involved in framing such research; given that there is evidence for gender differences in nicotine sensitivity and metabolism, such investigations are likely to be informative. How cognitive changes which may result from smoking affect such behaviors as dependency (Edwards & Raw, 1991) or the maintenance of addictive behaviors (Henningfield, Cohen & Slade, 1991;West &Gmnberg, 1991a) is still unclear. The interested reader is directed to two recent comprehensive collections of tobacco research (Baum & Grunberg, 1991; West & Gninberg, 1991b) for a thorough summary of major issues on these and related topics. To conclude, while cigarette smoking may have a positive effect upon the performance of simple repetitive tasks, it appears to have a negative effect upon the performance of tasks with high demands upon problem-solving skills supported by LTM and working memory. This negative effect is not overwhelming but under heavy task demands, the magnitude of the deficit increases. Based upon the

1324

George J. Spilich et al.

results of the present study, it is clearly premature to either conclude that smoking 'has positive benefits for behavior efficiency' (Edwards et al, 1985); 'facilitates . . . storage' (Warburton ei al., 1986); 'helps concentration' (Wesnes & Warburton, 1984) or to discuss 'the beneficial effects of cigarette smoking' (Wesnes, Warburton & Matz, 1983) on any but the most mundane and repetitive of tasks.

Acknowledgements The authors would like to express their appreciation to Ms Carolyn Naff, Mr Michael Johnson, Mr Bryan Kroll, and Ms Dianna Holden for assistance in data collection and manuscript preparation and to Griffith Edwards and three anonymous reviewers for helpful suggestions with the manuscript. Portions of these results were reported at the 1985 meeting of the Midwestern Psychological Association, the 1986 and 1991 meetings of the Eastern Psychological Association, and the 1987 meeting of the American Psychological Association.

term tobacco abstinence on complex versus simple mental tasks. Perceptual and Motor Skills, 42, pp. 413-414. ELLINGHAUS, C . C . (1983) The effects of cigarette smoking on memory and attention. Unpublished thesis, Washington College, Chestertown, MD. 21620. FLAMMER, A . & KiNTSCH, W. (Eds) (1982) Discourse Processing (New York, North Holland). FRANKENHAEUSER,

M . , MYRSTEIN,

A - L . , POST, B.,

JOHANSSON, G . (1971) Behavioral and physiological effects of cigarette smoking in a monotonous situation, Psychopharmacologia, 22(1), pp. i-7. FRASURE-SMITH, N . & RoLicz-WoLOSZYK, E. (1982) Memory problems after ischemic heart disease episodes: effects of stress, benzodiazepines and smoking. Journal of Psychosomatic Research, 26(6), pp. 613-622. FTC REPORT (1988) Tar, nicotine and carbon monoxide of the smoke of 272 varieties of domestic cigarettes. Report No. FO24149, December, Washington, DC. GoNZALES, M. A. & HARRIS, M . B. (1980) Effects of cigarette smoking in recall aad categorization of written material. Perceptual and Motor Skills, 50, pp. 407-410. GRUNBERG, N . E. & ACRi, J. (1991) Conceptual and methodological considerations for tobacco addictions research, British Journal of Addiction, 86(5), pp. 637-641. GRtmBERG, N., WINDERS, S. & WEWERS, M . E . (1991)

Gender differences in tobacco use. Health Psychology, 10(2), pp. 143-153. HEIMSTRA, N . W . , BANCROFT, N . R. & DEKOCH, A. R.

References ADAMS, J. R. & WILLIAMS, E. B. (1966) The association

(1967) Effects of smoking upon sustained performance in a simulated driving task. Annals of the New York Academy of Science, 142(1), pp. 295-307. HENNINGFIELD, J. E. (1984) Behavioral pharmacology of

between smoking and accidents: overdependency as an cigarette smoking, in: THOMPSON, T . , DEWS, P. B. & influencing variable. Traffic Quarterly, 20, pp. 583-588. BARRETT, J. E. (Eds) Advances in Behavioral PharmaANDERSSON, K . (1975) Effects of cigarette smoking on cology, 4, pp. 131-210. learning and retention, Psychopharmacologia, 41, pp. HENNINGFIELD, J. E., COHEN, C. & SLADE, j . (1991) Is 1-5. nicotine more addictive than cocaine? British Journal of BAUM, A. & GRLJNBERG, N . E. (Eds) (1991) Gender and Addiction, 86(5), pp. 565-569. health (Special issue). Health Psychology, 10(2). HILL, R. D . (1989) Residual effects of cigarette smoking BAUMAN, K . E., KOCH, G . G . & FISHEB, L . A. (1989) on cognitive performance in normal aging. Psychology Family cigarette smoking and test performance by and Aging, 4(2), pp. 251-254. adolescents. Health Psychology, 8(1), pp. 97-105. HOUSTON, J. P., SCHNEIDER, N . G . & JARVIK, M . E . (1978) CROWDER, R. G . (1979) Principles of Learning and Effects of smoking on free recall and organization, Memory (Hillsdale, NJ, Eribaum). American Journal of Psychiatry, 135(2), pp. 220-222. DlEHL, H. S. (1969) Tobacco and your Health (New York, KiNTSCH, W. & VAN DijK, T. A. (1978) Toward a model of McGraw-Hill). texi comprehension and production. Psychological ReDIFRANZA, J. R., WINTERS, T . H . , GOLPBERG, R. J., view, 85(5), pp. 363-394. CiRiLLO, L. & BILIOURIS, T. (1986) The relationship of KIRK, R. E. (1968) Experimental Design: procedures for the smoking to motor vehicle accidents and traffic violabehavioral sciences (Belmont, CA, Brooks-Cole). tions. New York State Journal of Medicine, 86, pp. KLEINMAN, K. M . , VAUGHN, R. L . & CHRIST,T. S. (1973) 464-467. Effects of cigarette smoking and smoking deprivation on DixoN, R. A., SIMON, E. W . , NOWAK, C . A. & Htn,TSCH, paired-associate learning of high and low meaningful D. F. (1982) Text recall in adulthood as a function of nonsense syllables. Psychological Reports, 32, pp. level of information, input modality, and delay interval, Journal of Gerontology, 37, pp. 358-364. 963-966. EDWARDS, G. & RAW, M. (1991) The tobacco habit as drug KNEZEVIC, S., MUBRIN, Z . , RISBERG, J., VUCINIC, G . , dependence, British Journal of Addiction, 86(5), pp. SPILICH, G . , GUBAREV, N . & WANNENMACHER, W . 483-488. (1989) Pyritinol treatment of SDAT patients: evaluaEDWARDS, J. A., WESNES, K . , WARBURTON, D . M . & GAIL, tion of psychiatric and neurological examination, psyA. (1985) Evidence of more rapid stimulus evaluation chometric testing, and rCBF measurements, InternaIbllowing cigarette smoking. Addictive Behaviors, tional Journal of Clinical Psychopharmacology, 4(1), 10(2), pp. 113-126. pp.25-28. ELGEROT, A. (1976) Note on selective effects of shortKRASNEGOR, N . A. (1979) Introduction, in: KRASNEGOR,

Cigarettes and performance

1325

and current controversies. Quarterly Journal of ExperiN. A. (Ed.) The Behavioral Aspects of Smoking, NIDA mental Psychology, 27, pp. 1-32. Research Monograph No. 26 (Washington, DC, US Printing Office). STEVENS, H . A. (1976) Evidence that suggests a negative association between cigarette smoking and learning LACHMAN, R., LACHMAN, J. L . & BUTTERFIELD, E. C . performance. Journal of Clinical Psychology, 32(4), pp. (1979) Cognitive Psychology and Information Process896-898. ing: an introduction (Hillsdale, NJ, Erlbaum), LESGOLD, A. & PERFETTI, C . A. (Eds) (1981) Inleractive

Processes in Reading (Hillsdale, N], Erlbaum). MACKWORTH, J. F . (1964) Performance decrement in vigilance threshold determinations and high speed motor tasks, Canadian Journal of Psychology, 18, pp. 209-223. MASSARO, D . W . (1989) Experimental Psychology: an information processing approach (New York, Harcourt Brace Jovanovich). McGuiRE, F. L. (1972) Smoking, driver education and other correlates of accidents among young males, Journal of Safety Research, 4, pp, 5-U. MILLER, J. R, & KINTSCH, W . (1980) Readability and

recall of short prose passages: a theoretical analysis. Journal of Experimental Psychology (Learning, Memory, and Cognition), 6(4), pp. 335-354. MuBRiN, Z., KNEZEVIC, S., SPILICH, G . J., RISBERG, ].,

GuBAREV, N., WANNENMACHER, W , & VuciNic, G. (1989) Normalization of rCBF patterns in senile dementia of Alzheimer's type. Psychiatry Research, 29, pp. 303-306. NEISSER, U . (1963) Decision-time without reaction-time: experiments in visual scanning, American Journal of Psychology, 76, pp. 376-385. NEISSER, U . (1964) Visual search. Scientific American, 210(6), pp. 94-102. NEWHOUSE, P . A., SUNDERI-AND, T . , TARIOT, P. N., BLUMHARDT, C . L . , WEINGARTNER, H . , MELLOW, A. &

MURPHY, D . L. (1988) Intravenous nicotine in Alzheimer's disease: a pilot study, Psychopharmacology, 95, 171-175. PEEKE, S. C. & PEEKB, H . (1984) Attention, memory, and cigarette smoking, Psychopharmacology, 84, pp. 205-216. RUSSELL, M., P E T O J . & PATEL, U . (1974) The classifica-

tion of smoking by factorial structure of motives. Journal of the Royal Statistical Society Series A: General, 137(3), pp. 313-346. SMITH, P. J. & LANGOLF, G . D . (1981) The use of

TURNER, A. & GREENE, E. (1977) The construction and use

of a propositional text base. Technical Report No. 63. University of Colorado, Boulder, CO, Institute for the Study of Intellectual Behavior. US DEPARTMENT OF HEALTH AND HUMAN SERVICES

(1988) The health consequences of smoking: nicotine addiction; A report of the Surgeon General, pp. 377-392. Rockville, MD, Centers of Disease Control, Office for Smoking and Health. ViPOND, D. (1980) Micro- and macroprocesses in text comprehension. Journal of Verbal Learning and Verbal Behavior, 19, pp. 276-296. Voss, J. F., TYLER, S. W . & BISANZ, G . L. (1982) Prose comprehension and memory, in: PUFF, C . R. (Ed.) Handbook of Research Methods in Human Memory and Cognition, pp. 349-393 (New York, Academic). VURPILLOT, E. (1968) The development of scanning strategies and their relation to visual differentiation, Journal of Experimental Child Psychology, 6, pp. 632-650. WALLER, j . A. (1986) On smoking and drinking and crashing, New York State Journal of Medicine, 86(9), pp. 459-460. WARBURTON, D . M . & WESNES, K . (1984) Drugs as

research tools in psychology: cholinergic drugs and information processing, Neuropsychobiology, 11, pp. 121-132. WARBURTON, D . M . , WESNES, K . , SHERGOLD, K . & JAMES,

M. (1986) Facilitation of learning and state dependency with nicotine, Psychopharmacology, 89(1), pp. 55-59. WECHSLER, D . (1945) A standardized memory scale for clinical uss. Journal of Psychology, 19, pp. 87-95. WEINGARTNER, H . (1985) Drugs that facilitate cognitive processes: characterizing the response. Drug Development Research, 5, pp. 25-38. WESNES, K . & REVELL, A. (1984) The separate and

combined effects of scopotamine and nicotine on human information processing, Psychopharmacology, 84, pp. 5-11.

WESNES, K . & WARBURTON, D . M . (1978) The effects of Stern berg's memory-scanning paradigm in assessing cigarette smoking and nicotine tablets upon human effects of chemical exposure. Human Factors, 23(6), pp. attention, in: THORNTON, R. E. (Ed.) Smoking Beha701-708. vior: Physiological and Psychological Influences, pp. SPILICH, G . J. (1983) Life-span components of text 131-147 (London, Churchill-Livingston). processing: structural and procedural differences. Journal of Verbal Learning and Verbal Behavior, 22, pp. WESNES, K . & WARBURTON, D . M . (I983a) Smoking, nicotine and human performance. Pharmacology and 231-244. Therapeutics, 2\, pp. 189-208. SPILICH, G. J. (1985) Discourse comprehension across the WESNES, K. & WARBURTON, D . M . (I983b) Effects of span of life, in: CHARNESS, N . (Ed.) Aging and Human smoking on rapid visual information processing perPerformance, p. 143-190 (New York, Wiley). formance, Neuropsychobiology, 9, pp. 223-229. SPILICH, G . J., VESONDER, G . T . , CHIESI, H . L . & Voss, J. WESNES, K . & WARBURTON, D . M . (1984) The effects of F. (1979) Text processing of domain-related informacigarettes of varying yield on rapid information processtion for individuals with high and low domain knowling performance, Psychopharmacology, 82(4), pp. edge. Journal of Verbal Learning and Verbal Behavior, 338-342. 18, pp. 275-290. STERNBERG, S. (1969) Memory scanning: mental proWESNES, K . , WARBURTON, D . M . & MATZ, B. (1983) Effects of nicotine on stimulus sensitivity and response cesses revealed by reaction-time experiments, American bias in a visual vigilance lask,Neuropsychobiology,9(_\), Scientist, 57, pp. 421-457. pp. 41-44. STERNBERG, S. (1975) Memory scanning: new findings

1326

George J. Spilich et al.

WEST, R. & GRUNBERG, N , E. (1991a) Implications of

tobacco use as an addiction, British Journal of Addiction, 86(5), pp. 485-488.

WILLIAMS, D . G . (1980) Effects of cigarette smoking on immediate memory and performance in different kinds of smokers, British Journal of Psychology, 71, pp- 83-90,

WEST, R. & GRUNBEBG, N . E. (Eds) (1991b) Future

YAMASHrrA, K., KOBAYASHI, S., YAMAGUCHI, S., KITANI,

directions in tobacco research. British Journal of Addiction, 86(5) (Special issue). WEST, R. & HACK, S. (1991) Effect of cigarettes on memory search and subjective ratings. Pharmacology, Biochemistry, and Behavior, 38, pp. 281-286.

M. & TsuNEMATSU, T. (1988) Effect of smoking on regional cerebral blood flow in the normal aged volunteers. Gerontology, 34, pp. 199-204.