Elsevier

Alcohol

Volume 25, Issue 3, November 2001, Pages 137-152
Alcohol

High-priority communication
Prolonged neurophysiological effects of cumulative wine drinking

https://doi.org/10.1016/S0741-8329(01)00191-4Get rights and content

Abstract

The effects of a single, large dose of alcohol have been studied extensively, but how alcohol affects the brain under more realistic social drinking situations has received scant attention. The neurophysiological effects of a cumulative dose of alcohol were investigated as subjects drank three glasses of alcoholic or placebo red wine, 1 h apart. In a double-blind procedure, electroencephalographic (EEG) activity was recorded for social drinkers during rest and performance of a working memory task at two levels of difficulty. Background EEG power in the theta, slow alpha, and beta bands increased with alcohol consumption. Along with this systemic increase in background cortical resonant activity, event-related potential (ERP) amplitudes decreased between 200 and 350 ms poststimulus and P300 latency increased, effects that occurred while relevant stimulus factors were being evaluated. These neurophysiological effects endured 3 h after drinking, whereas blood/breath alcohol concentration had decreased considerably and cognitive performance returned to normal. These findings seem to indicate that moderate social alcohol consumption has cumulative effects on brain function that persist for hours after chemical and behavioral indicators of intoxication have diminished. The results seem to indicate that neuronal populations needed for stimulus processing were less available after wine consumption (as evidenced by reduced ERP amplitudes) because of increased background oscillatory activity (as evidenced by increased background EEG power).

Introduction

Although the deleterious effects of alcohol on the mind and body are well known (e.g., Allebeck & Olsen, 1998, Bradley et al., 1998, Reid et al., 1999), alcohol may have beneficial effects as well (Rehm & Bondy, 1998). There is epidemiological evidence that moderate, even daily, consumption of alcohol can reduce the risk of heart disease Criqui, 1998, Simonetti et al., 1995. Alcoholic beverages, and red wines in particular, contain tannins, flavonoids, and other phenolic compounds that play a critical role in modulating important functions, such as oxidation and coagulation Goldberg et al., 1995, Puddey & Croft, 1999, Van Golde et al., 1999, Wolfort et al., 1996. On the basis of such findings, some physicians recommend that their patients drink a glass or two of wine daily for its cardioprotective effect Bello et al., 1994, Constant, 1997, Rimm et al., 1996.

Given the prevalence of alcohol as a social drug and its serious consequences, it is not surprising that its effects on brain function, cognition, and performance in human beings have been the focus of considerable research attention. Most of this research has focused on the effects of a single dose of a highly potent alcoholic drink Begleiter & Platz, 1972, Cohen et al., 1993a, Gevins & Smith, 1999, Heishman et al., 1997. However, alcohol is usually consumed in social settings in a cumulative fashion. Rather than drinking a single large dose of alcohol in a period of 10–20 min, as is the norm in laboratory studies, people more often consume a number of less potent drinks over a period of several hours (Dougherty et al., 1999). Hence, the effects of alcohol on brain and behavior under more realistic, cumulative dosing situations remain unclear.

In a typical social drinking situation, blood/breath alcohol concentration (BBAC) increases with each subsequent alcoholic beverage, peaking shortly after the last one is consumed. When drinking stops and subjective feelings of intoxication diminish, the drinker may believe that the effects of alcohol on his or her behavior and ability to think clearly decrease concomitantly. The reality is that behavioral performance and mental impairment can persist long after drinking has ceased. For example, hours after BBAC has peaked aggression levels remain elevated (Dougherty et al., 1999), psychomotor and driving performance remain impaired Ferrara et al., 1994, Seppala et al., 1976, and pilots continue to exhibit decreased performance in flight simulators Cook, 1997, Morrow et al., 1993, Yesavage & Leirer, 1986. To understand the effect of a typical social drinking situation on brain and behavior, it is therefore critical to study the effects of alcohol during both the peak and the descending portion of the BBAC curve. In the present study we sought to examine this issue by measuring neurophysiological and behavioral performance variables as healthy volunteer subjects drank red wine in a cumulative dosing procedure. Cumulative dosing procedures have been used in studies with animal as well as human subjects to assess the effects of drugs, such as codeine (Bertalmio et al., 1982) and marijuana (Chait et al., 1988). Such procedures have been used to assess the effects of alcohol as well Ando et al., 1987, DeWit et al., 1989, Dougherty et al., 1999 but not in studies that examined cognitive function or employed neurophysiological measures.

Even when performance measures do not change as blood alcohol levels increase, specific changes in the spectral composition of the background electroencephalographic (EEG) signal and in amplitude and latencies of event-related potential (ERP) peaks can still reveal whether brain function is affected by alcohol. Certain EEG signals, including spatially localized fluctuations in the theta (4–7 Hz) and alpha (8–12 Hz) frequency bands, are known to be sensitive to consumption of alcohol Ehlers et al., 1989, Gevins & Smith, 1999, Lukas et al., 1990, Mitchell, 1985. Results of previous EEG studies on the effects of alcohol have shown the most consistent effects in the alpha frequency band (Cohen et al., 1993b). Findings obtained from studies in which alpha was measured in a single, wide band have shown increases in alpha power with alcohol consumption Holmberg & Martens, 1955, Lukas et al., 1986. Results of studies in which alpha was divided into slow and fast bands (e.g., 8–10 and 10–12 Hz, respectively) have typically revealed an increase in slow alpha power and either a decrease or no change in fast alpha power Cohen et al., 1993b, Ehlers & Schuckit, 1991, Ehlers et al., 1989. Although the largest effects appear in the alpha band, alcohol tends to increase power of the EEG signal over a broad range of frequencies. Increases in delta, theta, and beta frequency power after alcohol ingestion have also been reported Ehlers et al., 1989, Gevins & Smith, 1999, Lukas et al., 1986. Alcohol also has an effect on ERPs, increasing the latencies (peak times) of early peaks associated with processing the physical attributes of a stimulus Alexandrov et al., 1998, Jaaskelainen et al., 1996, Krull et al., 1994, Seppalainen et al., 1981 as well as increasing latencies and decreasing amplitudes of later peaks associated with task-related cognitive processing Krull et al., 1993, Lukas et al., 1990, Murata et al., 1992, Porjesz & Begleiter, 1998.

The current study measured EEG activity, ERP, and behavioral performance variables in a naturalistic drinking exercise to assess the effects of alcohol during both ascending and descending limbs of the BBAC curve. Behavioral and ERP measures were taken during performance of a working memory task. Working memory refers to the ability of the brain to retain and manage internal representations for several seconds, so that they can be remembered or otherwise used (Baddeley & Hitch, 1974). This time- and capacity-limited function requires sustained focused attention, a process particularly sensitive to the effects of alcohol Gevins & Smith, 1999, Lemon et al., 1993, Millar et al., 1999, Vuchinich & Sobell, 1978. Results of studies of lesions seem to indicate that working memory depends on a number of cortical regions, including prefrontal and parietal cortex Frisk & Milner, 1990, Goldman-Rakic, 1987, Owen et al., 1990, Petrides & Milner, 1982. Because alcohol abuse and even social drinking have been associated with neuronal loss in various cortical regions (Harper, 1998), including the frontal lobes Cala & Mastaglia, 1980, Fein et al., 1995, Freund & Ballinger, 1988, Kato et al., 1991, alcohol may interfere with the brain regions required for efficient working memory function.

To assess working memory function, the current study used a spatial N-back task. This task requires comparing information held in working memory to new information being presented, as the information being retained or discarded is continually updated. Increasing the “N” in the N-back task increases the number of items to be remembered and the length of time they need to be remembered. Increasing difficulty by changing from a 0-back (compare the current stimulus to the first stimulus in a block of trials) to a 2-back (compare the current stimulus to the stimulus 2 trials ago) task typically results in decreased accuracy, increased reaction time (RT), or both. A number of neurophysiological changes are also commonly observed Gevins et al., 1994, Gevins et al., 1997, Gevins et al., 1998, McEvoy et al., 1998, Smith et al., 1999. As task difficulty increases, power in the theta band over frontal midline cortical sites tends to increase. Frontal midline theta appears to be generated in the anterior cingulate cortex (Gevins et al., 1997), a region critical for attention-demanding task performance Posner & Peterson, 1990, Posner & Rothbart, 1992. The increase in frontal midline theta with task difficulty supports the suggestion that increased utilization of systems and circuits involved in sustaining focused attention is required in the N-back task as N increases Gevins et al., 1997, Posner & Peterson, 1990, Posner & Rothbart, 1992. Power in the alpha band over dorsolateral frontal and parietal cortical sites decreases as task difficulty increases. Because alpha desynchronization has been interpreted as an electrophysiological correlate of activated cortical areas Niedermeyer, 1993, Pfurtscheller et al., 1996, this decrease in alpha power seems to indicate that more neurons are actively engaged in the N-back task as task difficulty increases.

In sum, the changes in mental effort caused by the task difficulty manipulation in the N-back task are reflected in specific EEG signals, such as parietal and frontal alpha and frontal midline theta rhythms. Alcohol ingestion, meanwhile, produces more anatomically widespread, systemic EEG changes, enhancing power across a broad frequency spectrum. Measuring EEG activity before and after alcohol consumption, during the performance of easy and difficult versions of a working memory task, can elucidate whether the diffuse neurophysiological effects of alcohol interact with the ability of the brain to respond to increasing cognitive demands. Further, ERPs can reveal how alcohol affects the ability to extract, recognize, and interpret task-relevant stimulus information. To examine the effects of social drinking on cognition, we examined neurophysiological and behavioral performance variables as social drinkers performed different difficulty levels of the N-back task during the consumption of a cumulative dose of alcoholic red wine. In the control condition, identical measures were taken as subjects drank a cumulative dose of a placebo nonalcoholic red wine. Testing intervals lasted 7 h, so that the effects of alcohol could be assessed during both ascending and descending portions of the BBAC curve.

Section snippets

Subjects

Eight social drinkers, ranging in age from 23 to 33 years, were recruited through advertisements placed in local newspapers. Social drinkers were defined as those who reported drinking at least one alcoholic beverage, but no more than 10 alcoholic beverages, per week. Subjects were excluded if they or any family member ever had a dependence on alcohol or any other drug of abuse. Medical and drug use histories were obtained from each subject to determine eligibility in the study. Negative

Blood/breath alcohol concentration

Subjects became more intoxicated after drinking each successive glass of alcoholic red wine. Fig. 1 illustrates how mean ± S.E.M. BBAC peaked at .038 ± .007, .072 ± .007, and .100 ± .006 grams per 210 liters of breath after wine consumption that preceded Intervals 2, 3, and 4, respectively. Readings declined after consumption of the third glass of wine, as BBAC decreased linearly from its peak in Interval 4 to .029 ± .004 grams per 210 liters of breath during Interval 7. Breathalyzer readings

Behavioral effects of alcohol

Both objectively and subjectively, subjects became progressively more intoxicated as they drank the three glasses of alcoholic wine. The BBAC increased by approximately .03 grams per 210 liters of breath per hour when subjects were drinking and then decreased at a rate of approximately .02 grams per 210 liters of breath per hour after drinking stopped. Self-reported ratings of drunkenness and impairment increased with each glass of wine and decreased at a more gradual rate after drinking

Acknowledgements

This research was supported by the National Institute on Alcohol Abuse and Alcoholism, grant #R44 AA11702, and the National Aeronautics and Space Administration, grants #NAG5-6349 and #NAG5-4915. We gratefully acknowledge the dedicated effort of Jennie Barber during data acquisition and analysis and the contributions of Drs. Halle Brown, Linda McEvoy, and Michael Smith to this project.

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