Effects of Morphine on Temporal Discrimination and Color Matching: General Disruption of Stimulus...

EFFECTS OF MORPHINE ON TEMPORAL DISCRIMINATION AND COLOR MATCHING:GENERAL DISRUPTION OF STIMULUS CONTROL OR SELECTIVE EFFECTS ON TIMING?

RYAN D. WARD AND AMY L. ODUM

UTAH STATE UNIVERSITY

Discrepant effects of drugs on behavior maintained by temporal-discrimination procedures makeconclusive statements about the neuropharmacological bases of timing difficult. The currentexperiment examined the possible contribution of a general, drug-induced disruption of stimuluscontrol. Four pigeons responded on a three-component multiple schedule that included a fixed-interval2-min, temporal discrimination, and color-matching component. Under control conditions, responserates and choice responses during the first two components showed evidence of control by time, andaccuracy for color matching was high in the third component. Morphine administration flattened thedistribution of fixed-interval responding and produced a general disruption of accuracy in thetemporal-discrimination component, whereas accuracy in the color-matching component was relativelyunaffected. Analysis of the psychophysical functions from the temporal-discrimination componentindicated that morphine decreased accuracy of temporal discrimination by decreasing overall stimuluscontrol, rather than by selectively affecting timing. These results suggest the importance of determiningthe neurophysiological bases of stimulus control as it relates to temporal discrimination.

Key words: morphine, timing, stimulus control, temporal discrimination, key peck, pigeons

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The neurophysiological processes underly-ing temporal regulation of behavior andaccurate discrimination of temporal durationhave been of increasing interest in recentyears. Research with both humans and nonhu-mans has led to the formation of severaltheoretical accounts that attempt to explainthe environmental and neurophysiologicalunderpinnings of accurate temporal discrimi-nation. For example, prominent theoreticalaccounts of the neurophysiological basis oftiming, such as the generalized timing model(e.g., Matell, Meck, & Nicolelis, 2003), hypoth-esize elaborate neurologically based informa-tion processing systems. According to thesemodels, accurate discrimination of duration isgoverned by internal-clock mechanisms com-

posed of pacemakers and accumulators. Basedon input from these systems interacting withmemory for recent temporal events, an organ-ism is able to accurately discriminate andrespond based on temporal stimuli.

Although models of temporal processinghave led to productive research aimed atdescribing the neuroanatomical correlates oftemporal discrimination (e.g., Gibbon, Mala-pani, Dale, & Gallistel, 1997; Meck, 1996),conclusive statements about the neural andbiochemical basis of timing remain elusive(see Gibbon et al., 1997). A growing body ofresearch has provided support for the role thatdopamine and other neurotransmitters play inaccurate timing of relevant temporal events(e.g., Buhusi, 2003; Hinton & Meck, 1997;Meck, 1996). In spite of these advances,further work is needed to understand moreprecisely how neuropharmacological and be-havioral processes contribute to accuratediscrimination of temporal stimuli (see Ri-chelle & Lejuene, 1998).

To complicate matters, a growing number ofdiscrepant findings have been reported inwhich the same drug, or drugs from the samepharmacological class, produced differenteffects on behavior maintained by a variety oftemporal-discrimination procedures (e.g.,Chiang et al., 2000; Frederick & Allen, 1996;Knealing & Schaal, 2002; Odum, Lieving, &Schaal, 2002; Santi, Coppa, & Ross, 2001). For

The authors thank Jason Martin for his assistance in thecomputer programming and conduct of this experiment,as well as Timothy Shahan and Christopher Podlesnik fortheir comments on a previous draft of this manuscript.Clive Wynne, Erin McClure, and Katie Saulsgiver providedvaluable suggestions with data analysis and helpful com-ments on a previous draft of this manuscript. Portions ofthese data were presented at the 2001 annual meeting ofthe Southeastern Association for Behavior Analysis inWilmington, North Carolina and the 2002 annual meetingof the Association for Behavior Analysis in Toronto,Canada.

Address correspondence to Ryan Ward or Amy Odumat the Department of Psychology, 2810 Old Main Hill,Utah State University, Logan, Utah 84322-2810 (e-mail:[email protected] or [email protected]).

doi: 10.1901/jeab.2005.94-04

JOURNAL OF THE EXPERIMENTAL ANALYSIS OF BEHAVIOR 2005, 84, 401–415 NUMBER 3 (NOVEMBER)

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example, some researchers have reported thatamphetamine results in overestimation of time(e.g., Chiang et al., 2000; Meck, 1996), whereassome have found generalized disruption oftiming or even underestimation of time (e.g.,Chiang et al., 2000). The reasons for thesediscrepant results are unclear. To date, anal-yses have suggested that variables such asspecies, sex, route of drug administration,and procedural variations cannot fully accountfor the discrepant outcomes (Cevik, 2003;Odum, 2002; Odum et al., 2002; Odum &Ward, 2004).

One possible explanation for these discrep-ant results is that drug administration resultsin a general decrease in discrimination of alltypes of stimuli, rather than in selectivechanges in the neuropharmacological me-chanisms responsible for timing. If this werethe case, then, following drug administration,choice responses in temporal-discriminationprocedures may no longer be under thefunctional control of the presented sampledurations. In fact, drugs have been reported toaffect performance on a variety of discrimina-tion procedures. For example, in one early studyBerryman, Cumming, Nevin, and Jarvik (1964)reported that sodium pentobarbital dose-de-pendently decreased accuracy in a color match-ing-to-sample task in pigeons. In a more recentstudy, Andrews and Holtzman (1988) assessedthe effects of morphine and amphetamine onperformance in a visual discrimination pro-cedure in rats. In their procedure, responses toone of two levers were reinforced if a stimuluslight had been briefly flashed above the lever atthe beginning of the trial. In this procedure,although amphetamine had relatively littleeffect, morphine produced a dose-dependentdecrease in accuracy.

In addition to these studies, others havereported that drugs from a variety of pharma-cological classes have disrupted performanceon discrimination procedures in rats (e.g.,Grilly, Genovese, & Nowak, 1980; Koek &Slangen, 1983, 1984), pigeons (e.g., Berryman,Jarvik, & Nevin, 1962; Eckerman, Lanson, &Berryman, 1978; Picker, Massie, & Dykstra,1987), and monkeys (e.g., Dykstra, 1979;Ridley, Baker, & Weight, 1980). These results,when considered along with the discrepantresults in the timing literature mentionedabove, suggest the importance of experimentalpreparations and methods that clearly can

distinguish selective effects of drugs on timingfrom effects that occur as a result of a moregeneral disruption of stimulus control.

Few studies have attempted to assess simul-taneously the effects of drugs on accuracy oftemporal and other types of discriminations.Santi, Weise, and Kuiper (1995) assessed theeffects of amphetamine on performance ona temporal discrimination and a visual sym-bolic matching-to-sample procedure in pi-geons. Amphetamine disrupted accuracy fortemporal discrimination more than accuracyfor symbolic matching-to-sample. In addition,contrary to prominent theoretical predictions(e.g., Meck, 1996), amphetamine did notproduce overestimation of time. Santi et al.suggested that their results were due todisruption of attention to the temporal samplestimuli rather than selective changes in timing.

The present experiment further examinedhow drugs simultaneously affect the stimuluscontrol engendered by temporal and colorsamples. We used a multiple schedule in whichwe assessed the effects of morphine onperformance during fixed-interval, temporaldiscrimination, and color-matching compo-nents. Morphine was used because it has beenshown to disrupt performance in a temporal-discrimination procedure (e.g., Odum &Ward, 2004) and also has been shown todisrupt performance in a visual discriminationprocedure by decreasing the discriminabilityof the sample stimuli (Koek & Slangen, 1984).We reasoned that if the neuropharmacologicaleffects of morphine are specific to timing,then we should see clear disruption oftemporal discrimination, with little or nodisruption of color matching. If, however,morphine produces a general disruption instimulus control, then we should see changesin accuracy for color matching as well astemporal discrimination. In addition, perfor-mance during the temporal-discriminationcomponent was analyzed using a methodsuggested by Blough (1996), which can distin-guish drug effects due to changes in timingfrom those effects due to disruption ofstimulus control.

METHOD

Subjects

Four experimentally naive White Carneaupigeons served as subjects. Pigeons were

402 RYAN D. WARD and AMY L. ODUM

maintained at 80% 6 15 g of their free-feeding weight by postsession feeding asneeded. Between sessions, pigeons wereindividually housed in a temperature-controlled colony under a 12:12 hr light/dark cycle and had free access to water anddigestive grit.

Apparatus

Four BRS/LVE sound-attenuating chamberswere used. Chambers were constructed ofpainted metal with aluminum front panels.The chambers measured 35 cm across,30.7 cm deep, and 35.8 cm high. Each frontpanel had three translucent plastic keys thatcould be lit from behind with red, green,yellow, and blue light. Keys also could be litwith a variety of horizontal and vertical linestimuli, and required a force of at least 0.10 Nto record a response. Keys were 2.6 cm indiameter and 24.6 cm from the floor. A lamp(28 V, 1.1 W) mounted 4.4 cm above thecenter key served as a houselight. A rectangu-lar opening 9 cm below the center key pro-vided access to a solenoid-operated hopperfilled with pelleted pigeon chow. Duringhopper presentations, the opening was lit withwhite light and the houselight and keylightswere extinguished. White noise and chamberventilation fans masked extraneous noise.Contingencies were programmed and datacollected by a microcomputer located in anadjacent room using Med AssociatesH interfac-ing and software.

Procedure

Pretraining. Experimental sessions oc-curred 7 days a week at approximately thesame time. Following magazine training, thepigeons were exposed to an autoshapingprocedure (Brown & Jenkins, 1968). Duringthese sessions, all key colors and stimuli werepresented in the key locations in which theywould appear during the experiment. Follow-ing three sessions of autoshaping, the pigeonsreliably pecked all key colors and stimuli to beused in the experiment. Key pecking was thenmaintained on a fixed-interval (FI) schedule offood delivery of progressively increasing dura-tion until an FI 2-min schedule was reached.During these sessions, the center key was litwith three black vertical lines on a whitebackground. The FI 2-min schedule was in

effect for six sessions prior to multiple-sched-ule training.

Multiple schedule training. The procedurewas a three-component multiple schedule thatincluded FI 2-min, temporal discrimination,and color-matching components. During ini-tial training, these components were pre-sented in random order with the requirementthat each be presented 14 times during thesession and no component occur more thantwo times in a row. Components were separat-ed by a 30-s intercomponent interval (ICI)during which all keylights and the houselightwere extinguished. Pecks to the keys duringthe ICI had no programmed consequences. Toallow time for drug absorption prior toselected sessions, all sessions began with a 10-min chamber blackout. Following the black-out, the houselight and center key were lit tobegin the session. Temporal discriminationand color-matching components were preced-ed by the lighting of the center key with threeblack horizontal lines on a white background.This key served as a trial-ready stimulus toensure that the pigeon was attending to thesample. A peck to the center key randomlyproduced either a temporal discrimination orcolor-matching trial.

Temporal-discrimination component. A peckto the center key darkened the keylight andturned off the houselight for a period of 2 or8 s. This blackout duration constituted thetemporal sample for each trial. Sample dura-tions were randomly selected each trial withthe constraint that each sample duration bepresented an equal number of times duringthe session. Following the sample presenta-tion, the left and right keys were lit differentcolors, each color corresponding to eithera short or a long sample duration. Thelocation of each color (left or right key) wasrandomly determined from trial to trial (e.g.,Stubbs, 1968). A peck to the key that was thecolor that corresponded to the duration of thetemporal sample (short or long) resulted in 3-saccess to food. A peck to the key that was theother color produced a 3-s blackout. Key colorswere counterbalanced across pigeons in caseof a systematic drug-induced color bias (see,e.g., Wenger, McMillan, Moore, & Williamson,1995). For Pigeons P211 and P212, the colorsduring the temporal-discrimination compo-nent were green and red. For P211, greencorresponded to a short sample duration and

TEMPORAL DISCRIMINATION AND COLOR MATCHING 403

red to a long duration. This color assignmentwas reversed for P212. For Pigeons P213 andP214, the colors during the temporal-discrim-ination component were blue and yellow. ForP213, yellow corresponded to a short sampleduration and blue to a long duration. Thiscolor assignment was reversed for P214.

Color-matching component. A peck to thecenter key extinguished the trial-ready stimu-lus and lit the key with a color sample for 2 s.The center key then was extinguished and theside keys were lit different colors. The locationof each color (left or right key) variedrandomly from trial to trial. A peck to thekey that matched the sample color led to 3-saccess to food, and a peck to the key that didnot match the sample color led to a 3-sblackout. Key colors during this componentwere counterbalanced. For Pigeons P211 andP212, the colors during the color-matchingcomponent were blue and yellow. For P213and P214, the colors were green and red.

FI component. The center key was lit withthree black vertical lines on a white back-ground. The first peck after 2 min resulted in3-s access to food.

After color-matching and temporal discrim-ination accuracies were at least 80% over thelast 10 sessions, intermediate sample durationsof 3, 4, 4.5, 5.5, 6, and 7 s were inserted intothe temporal-discrimination component. Sam-ple durations of less than 5 s were consideredshort and sample durations of more than 5 swere considered long. Correct categorizationof the intermediate sample durations wasreinforced. A 3-min limited hold was institutedduring each component. If a response did notoccur within 3 min, all keylights and thehouselight were extinguished and a 30-s ICIoccurred, after which a new component wasrandomly selected. The number of componentpresentations of each type was changed toeight FI, 40 temporal discrimination, and eightcolor-matching components. Each temporalsample duration was thus presented five timesduring each session. Sessions ended after 56trials or 90 min, whichever occurred first.Sessions usually ended after 56 trials inapproximately 70 min.

Correction procedure. During training, whentemporal discrimination or color-matchingaccuracy was low because of a pronouncedcolor or side bias, a correction procedure wasinstated. In this procedure, a peck to the

incorrect side key was followed by a 3-sblackout. The entire trial was then repeated,with the same sample duration or color, andthe side keys lit with the same colors in thesame positions. This process continued untila correct choice ended the trial in food. Allpigeons experienced the correction procedureat some point during training. The correctionprocedure was not in effect during the drug-testing phase.

Morphine Tests

Drug testing began for individual pigeonswhen accuracy in the temporal discriminationand color-matching components was high andstable and rates of responding and the indexof curvature (a measure of temporal pattern-ing; Fry, Kelleher, & Cook, 1960) during the FIwere stable (without any evident trend orunusual variability) as judged by visual in-spection over the last 10 sessions. Respondingmet these criteria within 112 to 164 sessions,across pigeons.

Morphine sulfate (Sigma) was dissolved in0.9% saline and administered in a volume of1.0 ml/kg of the 80% free-feeding bodyweight. Morphine and vehicle were adminis-tered via intramuscular injections into thebreast immediately before the pigeon wasplaced in the experimental chamber. Toaccustom the pigeons to the injection pro-cedure, they were given one to three pre-liminary injections of saline. Results of theseinjections were excluded from the analyses.

Following the preliminary injections, mor-phine and vehicle were given in the followingorder: 1.0 mg/kg, 3.0 mg/kg, 0.56 mg/kg,5.6 mg/kg, and saline. These doses werechosen because they produce a wide range ofeffects of morphine (e.g., Odum & Ward,2004). Tests were separated by at least threeconsecutive baseline sessions not preceded byan injection. The session immediately pre-ceding a morphine or vehicle session wasdesignated as a control session. Dose-effectcurves were determined with all doses beforeany dose was repeated. The effects of salineand each drug dose were determined fourtimes for each pigeon. Data from the colormatching and temporal-discrimination com-ponents during sessions preceded by drugadministration were included in analyses onlyif at least half of the presented components ofeach type were completed. For Pigeon P211,


data were excluded on these grounds for onesession following administration of 3.0 and5.6 mg/kg. For Pigeon P212, data were ex-cluded for one session following administra-tion of 3.0 mg/kg and for two sessionsfollowing administration of 5.6 mg/kg. ForPigeon P213, data were excluded for 5.6 mg/kg, as this pigeon responded during only onesession following administration of this dose.Data from all sessions were included forPigeon P214.

RESULTS

Figures 1 and 2 show the effects of mor-phine on FI performance. Figure 1 showsoverall response rates during the FI duringcontrol sessions and as a function of mor-phine. Saline had no systematic effect onoverall rates of key pecking. Morphine de-creased rates of pecking somewhat, althoughin some cases the decreases were relativelysmall. Figure 2 shows the index of curvature(Fry et al., 1960) for all pigeons during controlsessions and as a function of increasingmorphine dose. The index of curvature isa measure of the proportional distribution ofresponses across fixed intervals. Fixed intervalswere divided into ten 12-s bins. The number ofresponses that occurred in each bin wassummed across the session for the FI compo-nent. The index of curvature then wascalculated for each session using the followingformula from Fry et al. (1960):

I ~ 9R10 { 2 (R1 z R2 z R3

z . . . R9)=10R10,

where R1 is the total number of responsesoccurring in the first bin, R2 is the totalnumber of responses occurring in the first andsecond bin, R3 is the total number ofresponses occurring in the first, second, andthird bins, and so on until R10, which is thetotal number of responses occurring in allbins. Calculated in this way, the possible rangeof the index is 20.90 (if all responses occurredin the first bin) through 0 (if an equal numberof responses occurred in each bin) to +0.90 (ifall responses occurred in the last bin).

During control sessions, the index of curva-ture was positive, indicating that relativelymore responses occurred later in the interval.Saline had no systematic effect on the index.

Morphine dose-dependently decreased theindex of curvature for all pigeons, with thelargest decreases occurring for Pigeons P212and P213. The decrease in the index indicatesthat, under morphine, relatively more re-sponses occurred earlier in the intervalscompared to control performance.

Fig. 1. Mean pecks per minute during the FI 2-mincomponent as a function of morphine for each pigeon.Unconnected points show means for all control (C) andsaline (S) sessions. Lines connect points showing the meanacross doses of morphine. Vertical bars represent onestandard deviation above and below the mean.


Although control accuracy in both the colormatching and temporal-discrimination com-ponents was above 0.8, accuracy for temporal-discrimination was slightly lower than for colormatching. Because the level of stimulus con-trol during control conditions has been shownto moderate the disruptive effects of drugs(e.g., Ksir, 1975), we compared the effects ofmorphine on temporal discrimination andcolor matching at similar levels of control

accuracy. Figure 3 shows the proportioncorrect for the temporal discrimination andcolor-matching components as a function ofmorphine dose for each pigeon. Data shown

Fig. 2. Mean index of curvature (degree of temporalpatterning) during the FI 2-min component as a functionof morphine for each pigeon. See text for calculation.Other details as in Figure 1.

Fig. 3. Proportion correct during the color matching(unfilled circles) and portions of the temporal-discrimina-tion (filled circles) components as a function of morphinefor each pigeon. Points showing accuracy for temporaldiscrimination reflect only accuracy for trials with 2- and8-s sample durations. Points for temporal discriminationand color-matching accuracy are offset slightly on the xaxis for clarity. Other details as in Figure 1. Data are notshown for Pigeon P213 following administration of5.6 mg/kg morphine because this pigeon respondedfollowing only one administration of this dose.


from the temporal-discrimination componentreflect only trials with 2 and 8 s sampledurations. Control proportion correct in bothcomponents was between 0.8 and 1.0 for allpigeons. There was no systematic difference inaccuracy between the color matching andtemporal-discrimination components. Salinehad no systematic effect on accuracy in eithercomponent. Overall, morphine decreased ac-curacy during temporal-discrimination trials,whereas accuracy for color matching wasrelatively unaffected. This effect was lessapparent for Pigeon P211. Examination ofthe accuracy data with all temporal-discrimi-nation trials included showed that the overalleffects of morphine were the same, althoughthe overall level of accuracy for temporaldiscrimination remained below that for colormatching at all doses of morphine.

To assess whether the effects of morphineon accuracy during the temporal discrimina-tion and color-matching components werestatistically significantly different, a line wasfit using linear regression to the data relatingthe proportion correct in the temporal dis-crimination and color-matching componentsto the dose of morphine. Control and salinedata were excluded from this analysis. Datawere pooled across pigeons. The slope of thefunction relating proportion correct in thetemporal-discrimination component to thedose of morphine was 20.055, whereas theslope of the function for the proportioncorrect in the color-matching component was20.011. These slopes were significantly differ-ent, F(1,112) 5 12.60, p 5 0.00057, whencompared using analysis of covariance asdescribed by Zar (1999). These results showthat morphine decreased accuracy of discrim-ination of the temporal sample endpoints,whereas accuracy of color matching wasrelatively unaffected.

Figures 4 and 5 present a detailed analysis ofthe effects of morphine on performance in thetemporal-discrimination component. The datain Figure 4 are expressed as the mean pro-portion of responses to the long key color asa function of sample duration. The data werefit using a cumulative Gaussian function withfour parameters: upper and lower asymptotes,standard deviation (SD), and mean. The fitswere obtained with the SOLVER tool of theEXCEL 5.0 spreadsheet program. Blough(1996) noted that if the means of the fitted

functions are different, averaging functionscan lead to a reduction of the slope of themean function. To avoid this artifact, weaveraged the proportion long response datafrom each determination of each dose ofmorphine and fit one Gaussian function tothe average data from each dose for eachpigeon.

In an analysis of these functions first in-troduced by Heinemann, Avin, Sullivan, andChase (1969) and described in detail byBlough (1996), the parameters of the modelreflect three sources of error in discriminationprocedures: overall stimulus control, sensitivi-ty, and bias. The degree of overall stimuluscontrol is reflected in the range of thefunction (upper asymptote – lower asymp-tote). In the current temporal-discriminationprocedure, if stimulus control was perfect, thevalues of the upper and lower asymptoteswould be 1 and 0, respectively. The resultingrange of the function would be 1.0, indicatingperfect discrimination of the endpoints (2 and8 s) of the temporal sample continuum. TheSD is a measure of the slope of the functionand reflects the degree of sensitivity to thedifferences between the sample stimuli in theshort and long categories, with greater SDsindicating decreased sensitivity. The mean ofthe function is the duration at which theproportion of responses to the long key coloris .5 (the point of subjective equality; PSE).This parameter is a measure of the degree ofbias, and is affected by shifts in the psycho-physical curve. Leftward and rightward shiftsin the curve change the mean of the functionand indicate bias for the key color associatedwith short and long sample durations, re-spectively.

Figure 4 shows that the control data (toprow) were well described by the cumulativeGaussian functions, which accounted for anaverage of 99.3% of the variance acrosspigeons. The functions had an average meanof 4.7 s, indicating that pigeons accuratelydiscriminated the passage of time. Morphine(lower rows) tended to dose-dependently de-crease the proportion of long responsesfollowing long sample durations, with anincrease in variability in the functions andacross determinations at higher doses. Partic-ularly at higher doses, morphine also in-creased the proportion of long responsesfollowing short sample durations. In most


cases, the proportion of responses to the longkey color tended to increase as a function ofincreasing sample duration, a result thatindicates some control of choice behavior bythe temporal dimension of the stimuli. Inaddition, in most cases the functions remainedroughly ogival, albeit somewhat flattened,across increasing doses of morphine.

Figure 5 shows dose-effect curves of theparameters derived from fitting the functionto the mean proportion long response datafrom each pigeon. The left panel shows therange of the psychophysical curves duringcontrol sessions and as a function of mor-phine. During control sessions, the range wasbetween .80 and .97, indicating a relativelyhigh level of overall stimulus control. Saline

administration had no systematic effect on therange. Morphine dose-dependently decreasedthe range for all pigeons. This result indicatesa dose-dependent decrease in stimulus con-trol.

To determine the extent to which decreasesin stimulus control were responsible for thedecreased accuracy in the temporal-discrimi-nation component, we examined the effects ofmorphine on the measures of sensitivity andbias (i.e., SD and mean). Interpreting thesemeasures can be problematic because, asBlough (1996) noted, decreases in the rangealso can change the estimates of the otherparameters. Because of this relation betweenthese parameters, SD changes due to de-creased stimulus control are confounded with

Fig. 4. Mean proportion of responses to the long key color during control (top row) and morphine sessions (lowerrows) as a function of sample duration for each pigeon during the temporal-discrimination component. Dotted linesindicate the bisection of .5 responses to the key color corresponding to the long sample duration, and the duration (5 s)that was midway between the short and long sample duration categories. Vertical bars represent one standard deviationabove and below the mean. Data are not shown for Pigeon P213 following administration of 5.6 mg/kg morphinebecause this pigeon responded following only one administration of this dose.


those due to changes in sensitivity (see e.g.,Blough, 1996). To determine the actual effectsof morphine on sensitivity of temporal dis-crimination in this procedure, it is necessary toobtain an unconfounded estimate of the slopeof the function (i.e., SD). To obtain thisestimate, it is necessary to remove the in-fluence of changes in the range from theestimate of the SD. Accordingly, we employedan asymptote correction first introduced byHeinemann et al. (1969).

In calculating this correction, Heinemannet al. (1969) assumed that, given perfectstimulus control, the asymptotes of the psy-chophysical functions should fall at zeroand unity. They further suggested that

failure of the asymptotes to fall at theseexpected values indicates that choice behavioron some trials is not governed by thepresented stimuli but is instead governed bysome other, unspecified stimuli. The asymp-tote correction gives the probability of a re-sponse with the assumption that choice behav-ior on the current trial is governed by thesample stimuli. In other words, the correctiongives an estimate of the parameters of themodel with the assumption of perfect stimuluscontrol (i.e., range value of 1.0). The resultingestimate of the SD is considered to representa more accurate measure of the effects ofmorphine on sensitivity of temporal discrimi-nation.

Fig. 5. Parameter estimates from the fit of the cumulative Gaussian function (see text for details) to mean proportionlong pecks from the temporal-discrimination component for each pigeon as a function of morphine. The left columnshows the range (upper asymptote – lower asymptote) of the function. The center column shows corrected estimates ofthe standard deviation (SD) of the function. The right column shows corrected estimates of the mean of the function, orthe time at which .5 of the pecks were to the key color corresponding to the long category (point of subjective equality;PSE). Unconnected points show parameter estimates for control (C) and saline (S) data. Lines connect data pointsshowing parameter estimates across doses of morphine. Data are not shown for Pigeon P213 following administration of5.6 mg/kg morphine because this pigeon responded following only one administration of this dose.


The center column of Figure 5 shows the SDof the corrected psychophysical curves duringcontrol sessions and across doses of morphine.The control SD was 1.26 for all 4 pigeons,indicating relatively high sensitivity to thetemporal distribution of the sample stimuliin the short and long categories. Saline hadlittle effect on the SD with the exception ofa large increase for Pigeon P211. Morphineslightly increased the SD at some doses forsome pigeons and decreased it for others.Overall, morphine had no systematic effect onthe SDs. These results suggest that when theinfluence of overall stimulus control is con-trolled for, sensitivity of temporal discrimina-tion was not systematically affected by mor-phine.

In addition to changing the SD, increases ordecreases in the range also can affect theestimate of the mean. Therefore, the asymp-tote correction described above was appliedto obtain unconfounded estimates of themean. The right column of Figure 5 showsthe means of the corrected psychophysicalcurves during control sessions and acrossdoses of morphine. The control means werebetween 4.2 and 5.1 s, indicating accurateestimation of the passage of time. Administra-tion of saline had no systematic effect on themean. Across pigeons, morphine had nosystematic effect on the mean. These resultssuggest that when the influence of stimuluscontrol was controlled for, morphine did notsystematically shift the curves either to the leftor the right, indicating no systematic bias forthe key color associated with short or longsamples.

To examine further the effects of morphineon choice behavior in the temporal-discrimi-nation component, we calculated responselatencies. Table 1 shows the latencies to peckthe trial-ready stimulus and temporal-samplecomparisons during all control and salinesessions and as a function of morphine dosefor all pigeons. Under control conditions,pecks to the trial-ready stimulus occurred onaverage 1.5 to 4.3 s after the stimulus waspresented. Saline had relatively little effect onresponse latencies. Morphine increased theresponse latency and standard deviation for 3of 4 pigeons, particularly at the highest doses.For Pigeon P214, morphine had no apprecia-ble effect on the latency to respond to the trial-ready stimulus, and for Pigeon P211 morphinedecreased latency at the three lowest doses butincreased latency at the highest dose. Re-sponses to the temporal sample comparisonsunder control conditions usually occurredwithin 2.5 s of choice-key illumination. Salinehad relatively little effect on the latencies.Across doses, morphine had no systematiceffect on the choice-response latencies. Laten-cies decreased slightly for 2 pigeons (P211 andP212), and showed little change for the other2 pigeons. Taken together, these results showthat although morphine increased the latencyto peck the trial-ready stimulus at higherdoses, the latency to peck a short or longcomparison key was not affected.

DISCUSSION

The baseline performance in the FI andtemporal-discrimination components indicat-

Table 1

Mean latency (in seconds) for responses to trial-ready stimuli and temporal choice comparisonsduring all control and saline sessions and as a function of morphine dose for all pigeons.Numbers in parentheses are standard deviations of the mean. Data are not shown for PigeonP213 following administration of 5.6 mg/kg morphine because this pigeon responded followingonly one administration of this dose.

Subject Response Control Saline

Morphine dose

0.56 mg/kg 1.0 mg/kg 3.0 mg/kg 5.6 mg/kg

P211 Trial ready 2.37 (0.30) 2.44 (0.54) 1.51 (0.18) 1.32 (0.29) 1.21 (0.31) 4.71 (3.91)Choice 2.22 (0.21) 2.20 (0.11) 1.73 (0.06) 1.72 (0.16) 1.94 (0.27) 2.21 (0.14)


P213 Trial ready 3.20 (0.73) 3.02 (0.38) 3.36 (0.52) 2.10 (0.20) 5.05 (5.21)Choice 1.18 (0.13) 1.36 (0.31) 1.22 (0.11) 1.20 (0.15) 1.38 (0.21)



ed discriminative control of behavior by time.The index of curvature from the FI compo-nent was positive, indicating that relativelymore responses occurred later in the interval.This pattern of responding is typical of thatusually seen in FI-schedule performance (Fer-ster & Skinner, 1957). During the temporal-discrimination component, the functions fit-ted to the proportion long response data wereroughly ogival in shape, with an average mean(4.7 s) between the arithmetic and geometricmeans of the sample duration endpoints. Theparameters derived from fitting the cumulativeGaussian functions to the data (i.e., range, SD,mean) showed that under control conditions,choice behavior was under the control of thetemporal dimension of the sample stimuli. Inaddition, baseline proportion correct in thecolor-matching component was between .94and .98 for all pigeons, indicating relativelyhigh discrimination between the two samplecolors. These results show that baseline per-formance during each component of themultiple schedule was typical of perfor-mance when these procedures are arrangedseparately.

Morphine dose-dependently decreased theindex of curvature. This result is consistentwith results from other studies of the effects ofmorphine on FI performance (e.g., Odum &Schaal, 2000; Rhodus, Elsmore, & Manning,1974). Also similar to results from otherstudies, overall response rates during the FIwere decreased as a function of increasingmorphine dose (e.g., Odum & Schaal, 2000).

During the temporal-discrimination compo-nent, morphine decreased the proportion ofresponses to the key color corresponding toa long sample duration following long samplesand increased the proportion of long choicesfollowing short sample durations, especially athigher doses. Morphine also dose-dependentlydecreased the range of the psychophysicalfunctions, indicating a decrease in stimuluscontrol. Although morphine decreased themeasure of stimulus control, it did not havea systematic effect on the measures of sensitiv-ity or bias (i.e., SD and mean) once un-confounded estimates of these parameterswere obtained using the asymptote correction(Blough 1996; Heinemann et al., 1969). Thisresult indicates that administration of mor-phine was not associated with changes insensitivity and did not result in over or

underestimation of the duration of the tem-poral samples. Taken together, these resultsindicate that although morphine decreasedoverall stimulus control, choice behavior wasstill under the remaining discriminative con-trol of the temporal samples. Choice behaviorin the color-matching component was relative-ly unaffected by morphine administration.

Morphine decreased the index of curvatureduring the FI, which resulted partly fromincreases in response rates early in the intervaland partly from decreases in response rateslater in the interval. Response rate changes ofthis sort have been interpreted as reflectingoverestimation of time (e.g., Killeen, 1991;McAuley & Leslie, 1986; Meck, 1996). Howev-er, morphine produced no systematic effectson the measures of timing in the temporal-discrimination component. These apparentlyconflicting results can be resolved by appeal-ing to another interpretation of the effects ofdrugs on behavior maintained by FI schedules.Drug-induced changes in response rates canbe considered under the rubric of rateconstancy (e.g., Byrd, 1979, 1981; Gonzalez &Byrd, 1977). The rate-constancy concept statesthat drugs can reduce variability in behavior.As drug doses increase, response rates tend toconverge toward a more uniform rate. Thistype of convergence in response rates duringthe FI is what might be expected if adminis-tration of drugs resulted in a general loss ofstimulus control. Therefore, rather than beingconsidered as evidence of overestimation oftime, the response rate changes observed inthe FI component can be interpreted asresulting from a morphine-induced disruptionof stimulus control.

Somewhat surprising is the fact that mor-phine disrupted the measure of stimuluscontrol (i.e., accuracy) during the temporal-discrimination component, but had littleeffect on accuracy during the color-matchingcomponent. One possible explanation is thatthe effects of drugs on behavior maintained bydiscrimination procedures depend on thedifficulty of the discrimination. In the currentexperiment, the color-matching componentwas a matching-to-sample task, whereas thetemporal-discrimination component consistedof a symbolic matching-to-sample (SMTS) task.The conditional discrimination required inthe temporal-discrimination component couldbe considered more difficult and, therefore,


could have been more easily disrupted bymorphine.

Although this interpretation is appealing,the results of another experiment suggest itmay not be correct. In the study conducted bySanti et al. (1995), one trial type requiredpigeons to match short (2 s) and long (8 s)sample durations to red and green comparisonstimuli, whereas the second trial type requiredpigeons to match red and green samples tovertical and horizontal line comparisons. Bothtypes of trials consisted of SMTS tasks, yetamphetamine decreased accuracy during tem-poral-discrimination trials and not duringcolor-matching trials. Santi et al.’s resultssuggest that the selective disruption of tempo-ral discrimination in the current experimentwas not due to the more difficult nature of theconditional discrimination in the temporal-discrimination component.

Further consideration of the two discrimi-nation tasks used in the present experimentmay provide an answer. In the color-matchingcomponent, sample stimuli consisted of twocolors, whereas the temporal-discriminationcomponent presented a continuum of eightsample durations. Inspection of the controlpsychophysical functions (Figure 4) shows thatintermediate sample durations in the shortand long categories were not always catego-rized as such. This result is evidence ofstimulus generalization, which often occurswhen stimuli to be discriminated vary alonga continuum (e.g., Guttman & Kalish, 1956;see Honig & Urcuioli, 1981, for review). Thusbeing embedded in the context of thetemporal sample continuum could have ren-dered discrimination for the temporal sampleendpoints more easily disrupted by morphinethan discrimination of the two colors in thecolor-matching component. It is possible thathad color matching been assessed alonga continuum, we would have seen similarchanges in accuracy between the color match-ing and temporal-discrimination components.Future experiments should examine this pos-sibility.

One final possibility is that temporal dis-crimination may be more susceptible todisruption by pharmacological manipulationsthan color discrimination. The results of anexperiment by Bradley and Blough (1993)suggest that some categories of discrimina-tions may indeed be more easily disrupted by

drugs than others. In separate experimentalconditions, pigeons discriminated betweenwavelength and luminance samples, whichwere varied along a continuum in a SMTSprocedure. Morphine decreased accuracymore for discrimination of luminance thanfor discrimination of wavelength. In addition,morphine produced decreases of overall stim-ulus control during the luminance, but not thewavelength, condition. Thus the differentialeffect of morphine on accuracy in the color-matching and temporal-discrimination com-ponents in the present experiment may haveresulted partly from an increased vulnerabilityof temporal discrimination to the disruptiveeffects of morphine.

The results of the current experiment onceagain highlight the discrepancies in theliterature on the effects of drugs on timing.Specifically, our results suggest that the effectsof drugs on behavior maintained by sometemporal-discrimination procedures may havelittle to do with the neuropharmacologicalcorrelates of timing performance. Rather,disruption of temporal discrimination by somedrugs may be a result of a general decrease instimulus control. Decreases in stimulus controlalso have been observed when behavior main-tained by discrimination procedures is sub-jected to nonpharmacological disruption, suchas delivering food during the intertrial interval(e.g., Blough, 1998; Nevin, Milo, Odum, &Shahan, 2003). In addition, Sutton and Ro-berts (2002) reported results consistent witha loss of overall stimulus control when theyassessed temporal discrimination during a di-vided-attention task (Experiments 1 and 2),and when they illuminated a distracter lightduring probe trials in a temporal-discrimina-tion procedure (Experiment 3).

The similarities between the effects ofmorphine on the measure of stimulus controlin the current experiment and the reportedeffects of pharmacological and nonpharmaco-logical manipulations on measures of stimuluscontrol in other experiments suggest a com-mon mechanism underlying stimulus controlin temporal and other types of discrimina-tions. For example, attention to relevantdimensions of antecedent stimuli is consid-ered to be an important factor in theestablishment and maintenance of overallstimulus control (see McIlvane, Dube, &Callahan, 1996, for discussion). The decrease


in the measure of stimulus control observed inthe current experiment could be interpretedas resulting from a disruption of attention tothe sample stimuli (see Blough, 1996; Heine-mann et al., 1969; Santi et al., 1995). Adisruption of attention to the sample stimuli,however, likely would result in increasedchoice response latencies. The fact that choiceresponse latencies were not systematicallyaffected by administration of morphine (seeTable 1) may be problematic for this account.

The interpretation of the decreases inaccuracy during the temporal-discriminationcomponent in the present experiment asresulting from decreases in stimulus controlmust be tempered in light of the results fromthe color-matching component. A morphine-induced general disruption of stimulus controlwould be expected to decrease accuracyduring the color-matching component as well.That morphine had no apparent effect onaccuracy during this component is trouble-some for a stimulus control account of theseresults.

The asymptote correction used to derive themeasure of stimulus control in the presentexperiment has not been used widely in theanalysis of data from temporal-discriminationprocedures (but see Church & Gibbon, 1982).It is possible, therefore, that this method ofdata analysis may not be suitable to character-ize accurately the effects of drugs on behaviormaintained by temporal-discrimination proce-dures. Even so, the results from the temporal-discrimination component are meaningful onother grounds. Examination of the uncorrect-ed psychophysical functions (Figure 4) showsthat morphine administration flattened thefunctions, a result that indicates a generalizeddisruption of temporal discrimination. Thisdisruption was not accompanied by any sys-tematic leftward or rightward shifts in thefunctions, indicating that pigeons did not overor underestimate the duration of the samples.Thus the results of the present experiment,whether interpreted in terms of a decrease ofstimulus control or a disruption of timing, canbe added to the growing number of resultsthat appear to be discrepant with the predic-tions of current models of the neuropharma-cology of timing (e.g., Meck, 1996).

The results of the present experiment andanalysis suggest the utility of experimentalpreparations and data-analysis techniques that

can clearly separate the effects of drugs onstimulus control from their effects on timing.Although characterization of data in terms oftheoretical constructs (e.g., attention) will beultimately less informative than determiningthe underlying neurophysiological mechan-isms responsible for successful performanceduring discrimination procedures, such char-acterization may provide a bridge between thebehavioral and neuroscience disciplines in thesearch for the neurophysiological basis ofstimulus control. Experimental methods andtechniques developed in the field of neurosci-ence could be combined with the methodol-ogy already employed by behavioral research-ers to further reveal the neurophysiologicalfoundations of basic behavioral phenomena.Of particular importance in relation to theresults of the present experiment will be theisolation of those neurophysiological systemsresponsible for the establishment and mainte-nance of stimulus control during temporal-discrimination procedures. Perhaps this ave-nue will help to synthesize the so far un-resolved discrepancies in the timing literatureinto an accurate and complete account of theneuropharmacology of timing.

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Received August 27, 2004Final acceptance June 6, 2005


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