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Acute dose of alcohol affects cognitive components of reaction time to an omitted stimulus: differences among sensory systems

Rationale The possibility that moderate blood alcohol concentrations (BACs) may impair cognitive processes before disturbing motor functions has raised concern about the safety of BACs ≤80 mg/100 ml. Reaction time (RT) to the presentation of a
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  Psychopharmacology (2006) 184: 75  –  81DOI 10.1007/s00213-005-0237-7 ORIGINAL INVESTIGATION Oscar H. Hernández .Muriel Vogel-Sprott .Teresita C. Huchín-Ramirez .Fernando Aké-Estrada  Acute dose of alcohol affects cognitive components of reaction time to an omitted stimulus: differences among sensory systems Received: 25 May 2005 / Accepted: 17 October 2005 / Published online: 7 December 2005 # Springer-Verlag 2005 Abstract  Rationale:  The possibility that moderate bloodalcohol concentrations (BACs) may impair cognitive pro-cesses before disturbing motor functions has raised concernabout the safety of BACs  ≤ 80 mg/100 ml. Reaction time(RT)to thepresentation ofastimulusor tothe omissionofaregularly occurring stimulus has been fractionated into in-dependent premotor (cognitive) and motor (movement)components. It has been suggested that cognitive processesmay be impaired at lower BACs than are motor processes, but the effects of moderate rising and declining BACs onthese component RT measures have not been investigated. Objectives:  An omitted stimulus RT task was used to test the hypothesis that moderate rising BACs impair (slow) premotor RT (PMRT) when motor RT (MRT) remainsunaffected. The task included visual, auditory, and tactilestimuli to explore differences in sensory sensitivity to al-cohol.  Methods:  Thirtymalesocialdrinkerswererandom-ly assigned to three groups ( n =10) that received 0.62 g/kgalcohol, 0.8 g/kg alcohol, or a placebo (0 g/kg). All par-ticipantsperformedthetaskthreetimes:baselineandduringrising and declining BACs.  Results:  Comparisons of thealcohol and placebo groups showed rising BACs slowedPMRTand had no detectable effect on MRT. Impairment invisual PMRT occurred under both alcohol doses. AuditoryPMRTwasimpairedonlyunderthe0.8g/kgdose,andtactilePMRTwas unaffected.  Conclusions:  Cognitive functionsare impairedbymoderate increasingBACs thatdonot affect motor movement, and the tactile sensory system may berelatively insensitive to this impairment. Keywords  Alcohol .Premotor reaction time .Visual .Auditory .Tactile .Omitted stimuli Introduction In an effort to reduce alcohol-related accidents or injuries,many jurisdictions adopt a legal definition of intoxication basedonbloodalcoholconcentration(BAC),suchas80mgalcohol/100 ml, and penalize drinkers for driving or op-erating heavy equipment with BACs above this limit. Al-though more moderate blood alcohol levels might beconsidered safe, reviews of research on the performance-impairing effects of low and moderate doses of alcohol findthe evidence is unclear and conflicting (Holloway 1995;Mitchell 1985). It has been suggested that the failure toreliably detect impairment at some given BAC on activitiesresembling those that may be undertaken by drinkers may be due to the differences among the tasks in their stimulusand response requirements as well as the cognitive pro-cesses involved (Moskowitz 1984). Similar inconsistencies between the occurrence of impairment and BACs also areevident in more simple laboratory tasks, such as reactiontime (RT). A review of 23 RTstudies noted that 80% of thestudies observed impaired (slowed) RTat BACs of 70 mg/ 100 ml, but the BACs at which impairment was detectedranged widely, from 20 to more than 100 mg/100 ml(Holloway 1995). That review did not distinguish betweensimpleandchoiceRT.SimpleRTtaskspresentonestimulusthat requires one particular response, whereas choice RTtasks are somewhat more complex: at least two different stimuli are presented that require different responses, andthe information presented by the stimulus must be assessed before choosing a response. Mitchell ’ s (1985) review of the effect of an acute dose of alcohol on simple and on choiceRT concluded that choice RT is impaired at lower BACsthan is simple RT and led to the suggestion that cognitive O. H. Hernández ( * ) . T. C. Huchín-Ramirez .F. Aké-EstradaLaboratorio de Neurobiología,Centro de Investigaciones en Enfermedades Tropicales,Universidad Autónoma de Campeche,Campeche, Mexicoe-mail: ohhernan@mail.uacam.mxTel.: +1-981-8130171Fax: +1-981-8130171M. Vogel-Sprott Department of Psychology,University of Waterloo,Waterloo,Ontario, Canada   processes might be more sensitive to disruption by alcoholthan are simple motor responses.Thetimebetweenastimulusandaresponseiscommonlyassumed to reflect the sum of the duration of a series of mental and motor processes (Welford 1952). The source of the timing delay related to these processes has been de-termined by partitioning the total RT into premotor (cog-nitive) RT and motor (movement) RT (e.g., Botwinick andThompson 1966). Premotor RT (PMRT) is the amount of time required to perceive and interpret the stimulus anddecide on a response before any movement occurs. Motor RT (MRT) is the elapsed time associated with the executionof the response. This procedure of fractionating RT to the presentation of a stimulus has been applied to simple andchoice reaction tasks (Botwinick and Thompson 1966; Ito1997; Raynor  1998; Simmons et al. 2002). The results of  this research have consistently shown that an individual ’ sPMRT and MRT are not correlated and apparently detect different processes. These findings have also been con-firmed by research fractionating RT to the  omission  of arepetitive stimulus (Hernández et al. 2005). An omittedstimulus task presents a recurring stimulus that requires animmediate response to the omission of the stimulus. Al-though the omitted stimulus RT paradigm is somewhat uncommon, it bears a resemblance to some real-life sit-uations such as those requiring a reaction to the cessation of a flashing stoplight or to a missing beep on a heart monitor.The RT to an omitted stimulus is of considerable interest  because electrophysiological studies show that a brain po-tential accompanies the cessation of a train of stimuli that lastsforafewseconds(Bullocketal.1994;Hernándezetal.1999). This omitted stimulus potential (OSP) is a specialform of event-related potentials that are associated withcognition and considered to represent objective signs of moderately high-level brain processing (Ramón et al.2001).TheOSPappearsto reflectan “ expectation ”  becauseit occurs only after a train of stimuli ceases and shows atime-locked occurrence when measured from the due timeof the first missing stimulus (Karamürsel and Bullock 2000).Little research has examined the effects of alcohol onfractionated measures of RT. One exception is a study that administeredaplaceboandalowandhighdoseofalcoholtosocial drinkers on different days and tested the subjects on a60-min battery of various tasks, one of which was a visualchoice RT (Liguori et al. 1999). The total choice RT was partitioned into  “ recognition ”  or PMRT (i.e., the latency tolift a finger from home position) and MRT (latency of afinger press adjacent to the target light). The test battery wasadministered during declining BACs (57  –  47 mg/ 100 mlunder the low dose, and 97  –  92 mg/100 ml under the highdose). The low dose had no detectable effects, but the highdose slowed the PMRTcomponent and did not significantlychange the MRT. The failure to obtain alcohol effects under the low dose is difficult to interpret. It might be attributed tothe fact that the same subjects performed the test batteryunderbothdosesaswellasaplacebo,andimprovementwithtaskpracticemayhavemaskedthemilderimpairingeffectof the low dose. In addition, tests were only administeredduring declining BACs. Information about the effect of rising BACs was not obtained and could be important  because research on psychomotor skills indicates that theintensity of the effect of a given BAC is usually greater onthe ascending than on the descending limb of the bloodalcohol curve (Kalant et al. 1971; Vogel-Sprott and Fillmore1993).Studies on the effect of alcohol on RT have primarily been based on the presentation of visual stimuli and havenot explored possible differences in the sensitivity to al-cohol among visual, auditory, or tactile sensory modalities.A within-subject design using the same RT paradigm tomeasure PMRTand MRT to different sensory stimuli under a dose of alcohol could provide valuable new informationabout possible differences among sensory modalities insensitivity to alcohol, as well as the relative sensitivity toalcohol of cognitive and movement components of RT. Theomitted stimulus task may be particularly useful in this re-gard because it is considered to require additional cognitivefunctions, such as sustained attention and discrimination of thecessationofatemporalstimulussequence(Bullocketal.1994) that are not involved in choice RT tasks. Noresearch has testedtheeffectof alcohol onPMRTandMRT to an omitted stimulus. However, the possibility that cognitive processes are more sensitive to disruption byalcohol than are motor responses suggests that PMRT to anomitted stimulus should be impaired (slowed) by moderateor low BACs, whereas MRT may be unaffected. Given that the effect of rising BACs may be more intense than de-clining BACs, these effects should most likely be observedduring rising BACs. The present research tested these hy- potheses using fractionated measures of RT to an omittedstimulus. Different groups of social drinkers received either a placebo or one of two moderate doses of alcohol designedto generate peak BACs around 50 and 80 mg/100 ml, re-spectively. A mixed within-subject design was adopted inwhichallparticipantsineachgroupperformedthetaskwithvisual, auditory, and tactile omitted stimuli during risingand declining BACs. Method ParticipantsThirty right-handed Hispanic male college students with amean (SD) age of 19.8 (1.9) were randomly assigned to oneof three groups ( n =10). All were healthy and none had ahistory of nervous system diseases or motor disability. All participants volunteered for the study and were informedabout the procedures before providing informed consent.The experiment was reviewed and approved by the EthicsCommittee of the University of Campeche, Mexico.Apparatus and materials Omitted stimulus task   This task was identical to that usedin prior research to test PMRTand MRT to visual, auditory, 76  and tactile stimuli (Hernández et al. 2005). A pattern gen-erator (Grass mod. 10VPG) presented the visual stimuli ona monitor. The monitor presented a black-and-white check-erboard with 16 squares (5×8 cm each). The center of themonitor was placed 30 cm in front of a participant  ’ s eyesand 30 cm to the left or right side to use the peripheralvisual field of each eye. This is a version of the simpledetection paradigm used by others (Iacoboni and Zaidel1999, Barthélémy and Boulinguez 2002, Hernández et al. 2005). The generator, hidden from the participant  ’ s view,was triggered and stopped by an electrical stimulator (Grass S48). The stimulator released a pulse every 2 s(0.5 Hz), which reversed the black and white squares. Theelectrical stimulator also triggered the auditory stimuli,which were presented as 10-ms  “ clicks ”  at 2-s intervals toeither ear through headphones. The auditory thresholdswere determined and set at 20 times the threshold so that they would be clearly heard. Tactile stimuli were admin-istered at 2-s intervals by two disc electrodes (Grass F-E5SH) placed on the medial finger of the left or right hand.These electrodes were connected to the electrical stimula-tor (Grass S48) through a stimulus isolation unit (GrassSIU5). Tactile thresholds were determined for each handand set at 1.2 times the threshold, which was well belowthe pain threshold.The same responses were made to the termination of atrain of stimuli in each sensory modality. At the outset of atrial, a response key (key 1) was depressed with the thumbuntil the train of stimuli ceased. At this time, key 1 wasreleased, and key 2, placed 10 cm in front of key 1, wasdepressed. Both response keys were connected to AC am- plifiers(GrassP511).Eachstimulusaswellasreleasingand pressing the response keys generated clear changes involtage related to baseline, which were collected on-lineusing a computer fitted with an analog-to-digital converter (Biopac Inc.) and analyzed using AcqKnowledge software(Biopac Inc.). The computer recorded the time between thechanges in voltage associated with the last stimulus in thetrainofstimuliandtheresponsesonkeys1and2.Measureswere in milliseconds and were converted to fractions of asecond. PMRTwas the time between the occurrence of thelast stimulus and the release of key 1. MRT was the time between releasing key 1 and pressing key 2. A participant  ’ sPMRTand MRTwere recorded on each trial, separately for each sensory stimulus (visual, auditory, or tactile) in theomitted stimulus task.  Alcohol Use Disorders Identification Test (AUDIT)  Thisquestionnaire was developed by Babor et al. (1992) for theWorld Health Organization to identify persons whose al-cohol consumption has become hazardous or harmful totheir health. AUDIT is a 10-item screening questionnairewith replies scored from 1 (never) to 4 (always). Twoquestions deal with the typical amount and frequency of drinking, four questions concern excessive drinking andsymptoms of alcohol dependence, and four ask about prob-lems caused by alcohol. The maximum score on the ques-tionnaire is 40. Low scores are considered to be within theguidelines of normal usage. Scores ranging from 8 to 15 areconsidered to exceed these guidelines, and scores of 16 andhigher indicate hazardous use where help or treatment isneeded (http://www. ). All individuals com- pleted the questionnaire prior to participating in the study,and none was eliminated on the basis of his score.ProcedureSubjects were instructed to report to the laboratory at 8:45 a.m. on the day of the experiment in a fasting state(i.e., no food or any stimulant drink, such as tea, cola, or coffee, since the previous evening). They also agreed toabstain from alcohol for at least 72 h before their par-ticipation. Before the experiment commenced, participantscompleted the AUDIT, and the auditory and tactile thresh-olds and intensities were determined. Then the participant was seated in front of a table where the two response keyswere within easy reach. The task instructions were identicalfor each sensory modality. Participants were told to holddown key 1 at the beginning of each trial and immediately press key 2 when the train of stimuli ceased. Participantswore headphones during all tests andrested their heads onachin support that fixed their sight on a blue spot, 6.5 cm indiameter, on the wall 79 cm in front of their heads. Theywere instructed to maintain their gaze on the central fix-ation point at all times. Each trial was preceded by a verbal “ ready ”  signal. The number of stimuli in a train on a giventrial varied between 5 and 20 in a predetermined pseu-dorandom fashion. A test on the task presented 30 trials,with 10 consecutive trials administered with each type of stimulus. Because visual, tactile, and motor pathways arestrongly lateralized (Hellige 1993), potential laterality ef-fects were controlled by administering five trials withstimuli presented on the right side and responses with theright hand. The remaining five trials were presented onthe left side, again with uncrossed stimuli and responses.Although the auditory sensory system is not lateralized(Iacoboni and Zaidel 1999), the same procedure was usedwith auditory stimuli to standardize testing. Trials with agiven stimulus were completed in about 10 min and wereimmediately followed by trials with a different sensorystimulus. The order in which the sensory stimuli (visual,auditory, or tactile) were presented during a test wascounterbalanced in the groups. A test with all three sen-sory stimuli was completed in about 30 min.After the participants became familiar with the omittedstimulus task andthe stimuli, their zero BACswere verified by providing a breath sample to an Alco-Sensor IV(Intoximeters Inc., Mod. 13-0360-10, St. Louis, MO,USA). They then performed a pretreatment test. The results provided baseline measures against which to assess thechange in RT measures under treatment conditions.The groups then received their respective treatments. Allgroups received two drinks that were consumed within15 min. Two groups expected alcohol and received a mod-erate dose administered as standard vodka (40° GL) mixedwith orange juice in a ratio of one part alcohol to three parts juice. One group received 0.8 g/kg absolute alcohol. The 77  other group received 0.62 g/kg alcohol. These doses wouldresult in peak BACs of close to 80 and 50 mg/100 ml,respectively, and would occur approximately 60 min after drinking commenced. The third group served as a control.These participants also expected alcohol but received a placebo equal to the fluid equivalent of the alcohol drinks but containing only orange juice. Five milliliters of alcoholwas floated on the surface of each placebo drink, and theglasses were wiped with cotton soaked in vodka to enhancethe alcohol scent of the placebo beverage. This type of  placebohasfrequentlybeenfoundtoleaddrinkerstoexpect that alcohol had been received (e.g., Fillmore and Vogel-Sprott  1994, 1995). After the drinks were consumed, the participants re-mained at leisure for 15 min. Thirty minutes after drinkingcommenced, all participants ’  BACs were measured and atest on the omitted stimulus task was administered. Asecond BAC measured at 60 min was obtained when thetest was completed. An additional test occurred during the125- to 155-min interval andwas preceded andfollowed byBAC measures. After this test was completed, participantswere debriefed and received a standard snack. Those whoreceived alcohol remained at leisure in the laboratory untiltheir BACs had declined to a safe level.Data analysesScores were discarded on any trial where a responseoccurred before or coincided with the last stimulus in atrain.Intotal,0.5%ofthetrialscoreswererejected.Indrug-free experiments, it is common to trim RT data to eliminateoutliers and reduce the variability due to extraneous in-fluences (e.g., Van Selst and Jolicoeur  1994). However,someresearchontheeffectofalcoholsuggeststhatthedrugincreases the variance of RT and motor skill performance(Gustafson 1986a, b; Zack  1999). Because trimming RT data obtained on the treatment tests could possibly removean important drug effect, the data were untrimmed.On each test, a participant  ’ s PMRT and MRT wereaveraged on the trials with each sensory stimulus. Thedegree to which treatments changed each RT measure wasdetermined by subtracting a participant  ’ s baseline test scorefrom his score on each of the treatment tests. A positivechange indicated impairment (slower RT). The change inthe fractionated RT measures with each sensory stimuluscould be tested by a 3 (group) × 2 (RT) × 2 (test) analysis of variance (ANOVA). However, if alcohol increased thevariance of the measures, the assumption of homogeneityin the ANOVA would be violated and could lead to mis-leading conclusions. The homogeneity assumption waschecked by  F   tests of the variance ratios for the placebo andeach alcohol group. Significant ratios (  p  values <.01) in-dicating heterogeneity were obtained in the measures of change in PMRT and MRT (see  “ Procedural checks ” ).Thus, the prediction that PMRT would be impaired (slow-er) during rising BACs while MRT may show no signif-icant change was tested by planned comparisons betweenthe placebo and each alcohol group using adjusted  t   teststhat do not assume homogeneity of variances (Levine ’ stest, SPSS, 2001). Adjusted  t   tests were also used to assessalcohol effects during declining BACs. Results Procedural checksA one-way ANOVA of scores on the AUDIT questionnaireobtained no group differences (  F  2,27 =0.11,  p =.89). Themean (SD) scores for the 0.62 and the 0.8 g/kg alcoholgroups were 7.7 (3.5) and 7.0 (4.2), respectively. The meanfor the placebo group was 6.7 (6.3). Thus, the scores of thegroups were comparable and within the  “ safe drinking ” category. Replies to the questions concerning typical fre-quency and quantity of alcohol consumed showed that thesample (  N  =30) reported drinking a mean (SD) of 1.4 (1.0)times a month and 5 (3.1) drinks per occasion.The baseline test on the omitted stimulus task verifiedthat the performance of the groups did not differ prior totreatment. Separate one-way ANOVAs of the PMRT andMRT to the omitted stimulus in each sensory modalityobtained no group differences in PMRT (  p  values >.33) or MRT (  p  values >.45). Table 1 shows the baseline mean(SD) PMRT and MRT to the omission of visual, auditory,or tactile stimuli obtained in the combined sample (  N  =30).These results are consistent with those from drug-freeresearch using this task (Hernández et al. 2005).BACs were measured at 30, 60, 125, and 155 min after drinking commenced, just before and after each treatment test. The placebo group had zero BACs. The BACs of thetwo alcohol groups were analyzed by a 2 (dose group) × 4(time) ANOVA. Main effects of dose (  F  1,18 =16.1,  p =.001)and time (  F  3,54 =23.7,  p <.0001) were obtained. The inter-action was not significant (  F  3,54 =1.4,  p =.247). Figure 1shows the mean BAC of each group at intervals after drinking commenced. The BACs of the group receiving the0.8 g/kg dose was consistently higher than the groupreceiving the 0.62-g/kg dose. The BACs of both groupswere rising when the task was performed between 30 and60 min after drinking. When the task was performed duringthe 125- and 155-min interval, the BACs in both groupswere descending.The variance in the measures of change in PMRT of the0.8 g/kg group was significantly greater than the placebogroup with all sensory stimuli during ascending BACs andwith visual and auditory stimuli during descending BACs(  p  values <.01). The variance in PMRT change scores in Table 1  Mean (SD) baseline premotor and motor RT to visual,auditory, or tactile stimuli in the omitted stimulus task for the totalsample (  N  =30)StimuliVisual Auditory TactilePremotor RT (s) 2.62 (0.17) 2.48 (0.11) 2.69 (0.26)Motor RT (s) 0.43 (0.13) 0.41 (0.11) 0.45 (0.12)78  the 0.62-g/kg group also exceeded the placebo group ontests with visual stimuli during rising and descendingBACs and during rising BACs with auditory stimuli(  p  values <.01). The variance in MRT change scores of the 0.8 g/kg group was also greater than the placebo groupon tests with visual and auditory stimuli during risingBACs and the test with visual stimuli during decliningBACs (  p  values <.01). In view of the frequent occurrenceof significant heterogeneity in the measures of change inPMRT and MRT, planned comparisons between the placebo and each alcohol group used adjusted  t   tests that do not assume homogeneity of variances.Treatment effects Omitted visual stimuli  Planned comparisons of the changein the placebo group to each alcohol group supported thehypothesis that PMRT would be impaired during risingBACs. These results are illustrated in Fig. 2a.The positive change in PMRT of the 0.62-g/kg groupshows that it had become significantly slower than the placebo group ( t  = − 2.1,  df   =18,  p =.025, one-tailed), as hadthe 0.8 g/kg group ( t  = − 2.2,  df   =9.8,  p =.027). Although thefigure also indicates that PMRT was still slower in thealcohol groups than the placebo group on the test duringdeclining BACs, group comparisons were not significant for the 0.62-g/kg dose (  p =.14) or the 0.8 g/kg dose (  p =.28).The mean changes in MRT did not differ between the placebo and either alcohol group during rising (  p  values>.20) or during declining BAC tests (  p  values >.33). Themean (SD) change in MRT to omitted visual stimuli for the entire sample (  N  =30) showed a very slight improve-ment (faster RT) of   − 0.03 s (0.19) during the ascendingBAC test and  − 0.01 s (0.17) during the declining BACtest. Omitted auditory stimuli  The predicted slowing effect of rising BACs on PMRT was confirmed under the 0.8 g/kgdose ( t  = − 1.9,  df   =9.4,  p =.045). However, the change inPMRT under the 0.62-g/kg dose did not differ from the placebo (  p =.42). During declining BACs, the change inPMRTineachalcoholgroupdidnotdifferfromtheplacebogroup (  p  values >.26). Figure 2 b shows these results.Comparisons of the change in MRT showed no sig-nificant differences between the placebo and either alcoholgroup while BAC was rising (  p  values >.15) or declining(  p  values >.24). The sample (  N  =30) mean (SD) changein MRT with auditory stimuli was 0.030 s (0.13) and0.001 s (0.11) during tests of rising and declining BACs,respectively. Omitted tactile stimuli  Planned comparisons of the changein PMRT revealed no differences between the placebogroup and either alcohol group on tests during ascendingBACs (  p  values >.12) or declining BACs (  p >.40). Theentire samplemean (SD)change inPMRTwas0.11s (0.26)and 0.13 s (0.33), respectively. Group comparisons of thechange in MRTshowed that neither alcohol group differedfrom the placebo group during ascending (  p  values >.23) or descending BACs tests (  p  values >.33). The sample mean(SD) on each of these two tests was  − 0.03 s (0.12) and − 0.03 s (0.11). Time (min) 30 60 90 120 150 180    B   A   C   (  m  g   /   1   0   0  m   l   ) 30405060708090 0.62 g/kg0.80 g/kg Fig. 1  BAC as a function of time after drinking commenced ingroups that received 0.62 or 0.8 g/kg alcohol. The test duringascending BACs was performed between 30 and 60 min, and the test during declining BACs was performed between 125 and 155 min. Vertical bars  show SEMs    P  r  e  m  o   t  o  r   R   T   (  s   ) - Placebo0.62 g/kg 0.80 g/kg Ascending AscendingDeclining Declining AuditoryVisual *** a b Fig. 2  Mean change in PMRTon visual ( a ) and auditory ( b )tasks (in seconds) during as-cending and declining BACs inthe three groups that received a placebo, 0.62 g/kg alcohol, or 0.8 g/kg alcohol. Zero repre-sents the drug-free baseline. A positive score indicates impair-ment and a negative score in-dicates improvement.  Vertical bars  show SEMs79
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