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The Behavior Analyst Today

Volume 7, Number 4, 2006

An Automated Olfactory Discrimination Procedure with Rats

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Karen M. Lionello-DeNolf and Sheila M. Mihalick Although rats are commonly used as subjects in psychological research, few researchers have utilized their olfactory capabilities. An automated chamber capable of presenting multiple odor stimuli to 5 locations was used to train rats on 3 simple dis crimination and reversal tasks. Unique odor pairs were used for each discrimination and reversal task (Sets A, B, & C). All rats readily learned each task, taking longer to learn the reversal than the initial discrimination. Stimulus location did not influence accuracy, with only two exceptions. Moreover, rats showed no position biases for any of the 5 locations. These data demonstrate the feasibility of testing rats using olfactory cues in an automated apparatus with as many as 5 stimulus locations. This apparatus and procedure have potential applications to many areas of psychological investigation, including extra-dimensional shifts, compound stimulus training, and conditional discriminations. Key words: discrimination, olfactory, stimulus location, nose poke, rats

Rats are commonly used subjects in psychological research that are frequently tested on tasks that require bar pressing or maze running. Moreover, these tasks are typically used to examine associative, or discrimination, learning in rats. Few researchers, however, have supplanted these methodologies reliant on pressing and running behavior with those that take advantage of rats’ superior sense of smell. For example, a search of the abstracts on PsychINFO returned over 23,000 references using the keyword “discrimination,” but only 627 when the keywords “rat” and “discrimination” were combined. Utilizing odor cues in discrimination tests involving rats is advantageous because this species possesses a biological preparedness for learning about odors. For example, Nigrosh, Slotnick, and Nevin (1975) demonstrated that when responding was brought under control of redundant odor and tone cues, control of behavior was more effective with the odor cue (but see Neill & Harrison, 1987, for a discussion on the variables influencing auditory discrimination learning in rats). Moreover, developing reliable behavioral tests that take advantage of rodents’ olfactory sense has the potential to increase the utility of animal models of conditions, such as mental retardation, that are partially defined in terms of their behavioral effects (e.g, McIlvane & Cataldo, 1996). Nonetheless, the absence of utilizing olfactory stimuli in studies of discrimination learning remains notable. One possible reason is the inherent difficulty of working with them. Despite this, some researchers have attempted the challenge. Bunsey and Eichenbaum (1996) trained rats on matching to sample conditional discriminations using olfactory stimuli. Everyday household spices were mixed into sand and placed in small cups. Rats were required to dig into the cups to obtain reinforcement (a piece of chocolate). This procedure was effective in establishing reliable matching behavior. Moreover, the basic procedure has been replicated (Dudchenko, Wood, & Eichenbaum, 2000; Wood, Dudchenko, & Eichenbaum, 1999) and has been successfully modified for simple discrimination training with both rats and mice (Dusek & Eichenbaum, 1997; Mihalick, Langlois, Krienke, & Dube, 2000, respectively). Despite the success of this procedure, there are some disadvantages: a large number of scented cups need to be mixed prior to each session, the researchers have to manually present each stimulus during the session, and data have to be recorded by hand. Pena, Pitts and Galizio (2006) have taken this innovative idea further by conducting sessions in a standard operant chamber and streamlining the sand-cup delivery process. Baited sand cups are presented to the rats by sliding a tray that fits underneath the floor in and out of the chamber. This procedure involves less contact with the subjects during the session but still requires manual data recording. Using this procedure, Pena et. al have provided evidence for generalized identity matching to sample in rats. Other researchers have taken a different approach. Rather than mixing spices in sand, they have devised ways of delivering scented puffs of air directly into a nose poke aperture in the testing chamber.

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For example, Slotnick and colleagues (Lu, Slotnick, & Silberberg, 1993; Nigrosh, et. al, 1975; Slotnick & Katz, 1974) presented odors via an air stream pumped into a glass tube in which the rat was placed. A single odor could be presented at one time and rats were required to press or refrain from pressing a response key. Ramus and Eichenbaum (2000) have used a similar procedure to present odors directly into an operant chamber using a single odor delivery/nose poke port. These studies have been successful in establishing reversal learning sets trained via successive simple discriminations and in establishing conditional control by odor stimuli using successive matching to sample procedures. Strupp and colleagues have improved upon the single presentation location by expanding odor presentation to three locations in rats (Garavan, Morgan, Mactutus, Levitsky, Booze, & Strupp, 2000; Hilson & Strupp, 1997), and two locations in mice (Mihalick, Driscoll, & Strupp, 2001). Expanding stimulus presentation to multiple locations has been successful in establishing simple discrimination reversal performances in both species. One difficulty, however, is that these apparatuses are not commercially available. We wondered whether Strupp’s procedure with rats could be expanded even further. Specifically, we wanted to know whether training with five stimulus locations would result in successful discrimination performances, and we wanted to accomplish such training using an apparatus that is easily obtainable for other researchers. Increasing the number of available stimulus locations is desirable for several reasons. First, it expands the types of assessments that can be used to investigate psychological phenomena. For example, psychophysical work often involves determining the threshold of detection for various stimuli. With five odor presentation ports, differing concentrations of the same stimulus can be presented simultaneously, thereby increasing the sensitivity of the task to the animals’ ability. Second, recent stimulus control work has shown that training discrimination tasks with stimuli that are presented in a variety of locations increases the strength of control by the nominal stimulus (e.g., Lionello-DeNolf & Urcuioli, 2000). Finally, Sidman (1987) has pointed out that in conditional discrimination learning, two stimulus locations are insufficient for comparison and that three are necessary. The reason is that when a sample is presented in one location and the comparisons in the remaining two, there are difficulties in interpreting acquisition data: performances that appear to indicate the subject has learned the task may actually be reflecting quite different patterns of behavior such as control by stimulus location or exclusion. By expanding the number of locations, these possibilities are reduced if not eliminated. The purpose of this paper is to explore the feasibility of testing rats in an apparatus comprised entirely of commercially available parts. Up to six odors can be presented to any of five locations simultaneously. Rats were trained on a series of simple discrimination and reversal problems using all five locations. Method Subjects The subjects were three male and three female experimentally naïve Sprague-Dawley rats obtained from Charles River Laboratories. Five rats were approximately 90 days old at the start of the experiment. One female was a retired breeder of undetermined age. The male rats were housed in pairs in clear plastic tubs (one male was housed with a rat not included in this report because it died early in training). Two females were housed together and the retired breeder was housed alone. Each housing tub contained corn cob bedding, nestlets (white cotton squares), a plastic igloo toy for rodents (obtained from PetCo) and a water bottle that was continuously available throughout the experiment. The rats were housed in a room with a 12 hours on, 12 hours off light-dark cycle with lights on at 7 am. Upon arrival in the laboratory, rats were fed standard lab chow ad libitum for a period of one week. During that time, they were weighed daily. Free-feeding body weights were judged to be the average weight over three consecutive days during which the range of low to high weights was no greater

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than 10 g. At that point, each rat was placed on restricted feeding for approximately two weeks in order to gradually reduce its weight to 85% of its free-feeding value. Rats were run five days per week. At the end of each session, rats were returned to their home cage (if housed individually) or to a feeding tub (if housed in pairs) and were given their daily allotment of chow. The amount of chow was adjusted on a daily basis in order to keep rats at their target weights. Rats were given a minimum of two hours in which to eat the chow. After two hours had elapsed, rats that had consumed all the chow were returned to their home cage. If not all the chow was consumed, rats were given additional time to consume the chow. If the chow was not consumed by the end of the workday, the rat was returned to its home cage and the remaining chow was put in the home cage hopper. Rats were also fed in the feeding tubs on days in which sessions were not run. Apparatus The apparatus was a single operant chamber obtained from Coulbourn Instruments (Model # H10-11R-TC) surrounded by an isolation cubicle (Coulbourn Model # H10-23). The chamber measured 30.48 cm wide, 25.4 cm deep, and 30.48 cm in height. Two walls and the ceiling were made of aluminum whereas the remaining two walls were made of clear plastic. One of the clear walls was hinged and could be opened and closed to allow access to the inside of the chamber. The aluminum walls were fitted with modular pieces so that control devices could be mounted on the walls in various combinations. The floor was a standard grid shock floor (Coulbourn Model # H10-11R-TC-SF); however, the floor was not wired for electrical shock and no shock was delivered throughout the experiment. A blower fan (Coulbourn Model # H29005R), three 45 W house lights (Coulbourn Model # H11-01R), and a pellet feeder (Coulbourn Model # H14-22R-45) were located on one of the aluminum walls. A panel containing five nose poke openings (Coulbourn Model # 21-06R) measuring 2.5 cm in diameter was located on the wall directly across from the feeder (see Figure 1a and b). The nose poke holes were located 2.5 cm above the grid floor. Each nose poke opening was equipped with red, yellow, and green cue lights and with an odor/air delivery port. The inside hole consisted of white, reflective plastic and there was an invisible photobeam sensor (940 nM) located across each opening to detect responses. In order to increase the distance from the nose poke opening cut in the aluminum panel to the hole opening containing the photobeam, white PVC plastic was used to increase this area between .95 cm. As a result, the rat was forced to break the beam by inserting its nose further into the hole; otherwise, inadvertent photobeam breaks could occur as the rat merely sniffed near the port opening. An additional photobeam was mounted 2.54 cm in front of the nose poke panel. In addition, a hole was cut into one wall of the attenuating chamber and a dryer hose was attached in order to allow ventilation of the odors throughout the experimental sessions.

Figure 1-a.

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Figure 1-b.

Figure 1-c. Figure 1 a) Nose poke hole circuitry. Each nose poke odor nozzle received input from the jars containing the olfactory stimuli and the jar containing air. b) The nose poke panel. c) Olfactory stimulus control nodules connected to the odor jars and the nose poke hole nozzles.

Olfactory stimuli were contained in glass jars located next to the chamber. Each jar lid was equipped with two nozzles: one for clean air input and one for scented air output. Fresh air was fed into the jars by use of a standard aquarium pump (Tetra Whisper Air Pump 100 UL) and fish tank flexible vinyl tubing (The Pet Place Item # BRO 116). Tubing was also used to connect the jars to the nose poke odor/air delivery port and to the 12 olfactory stimulus control nodules (Coulbourn Model # H15-03) that controlled scent delivery (see Figure 1c). Finally, at the point of entry into the nose poke odor/air delivery port, each tubing line was fitted with a .32 cm liquid/gas check valve (United States Plastic Corp. Item # 64046) in order to prevent the scents from backing up into the tubes once the air source was turned off. Olfactory stimuli were everyday baking extracts (obtained from spicebarn.com): cinnamon, butterscotch, orange, almond, coconut, blueberry, and peppermint. Particular scents were chosen such that

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they were dissimilar from one another and such that the researchers all were able to detect them when presented in the apparatus. Each scent was mixed with propylene glycol to aid in stability. Scents were mixed on a daily basis in order to ensure the same potency from day to day. Each scent was measured in its own cylinder to prevent contamination with the other scents. Cinnamon was used during pretraining only. The remaining six scents were divided into three sets of two: butterscotch and orange (set A), almond and coconut (set B), and blueberry and peppermint (set C). Experimental events were controlled by a computer running Windows XP and Graphic State version 3.1 (Coulbourn) software. The computer was equipped with a PCI interface card (Coulbourn Model # H18-16) connected to a power base (Coulbourn H01-01) and 4 Habitest Lincs (Coulbourn # H02-08). Communication between the Lincs and the experimental equipment (e.g., the feeder, blower fan, olfactory control modules, etc.) was accomplished via 12 environment connection boards (Coulbourn # H03-04). Procedure Preliminary training. Preliminary training was designed to shape the nose poke response to each of the to-be-discriminated scents. On the first session, rats were given time to adjust to the experimental apparatus and to adapt to the pellet feeder. Rats were pla ced in the chamber and 45 mg Noyes pellets were delivered on a variable -time (VT) 5” schedule. The pellet feeder light was lit with every pellet delivery, and the houselights remained on throughout the session. A photobeam break was recorded when the rat made contact with the pellet. Rats were given one session to adapt to the pellet feeder. The next session was designed to train rats to orient to the wall containing the nose poke apparatus. At the beginning of a trial, the houselights were lit and once the rat broke the photobeam in front of the nose poke wall, a pellet was delivered. After each pellet delivery, there was an inter-trial (ITI) of 10 s in which two of the three houselights turned off. Each rat experienced one 60 trial session. During the third session, each rat was taught, by method of successive approximations, to poke its nose into a nose poke opening far enough to break the photobeam. There were 80 trials in this session and a poke far enough into any nose poke opening to break the photobeam was reinforced on each trial. Rats remained in this training phase until completing a session of 80 responses without the researcher having to reinforce any approximations of poking. Next, rats were reinforced for poking into a nose poke opening from which a cinnamon scent was emanating. If the rat did not begin responding after a few minutes, the method of successive approximations was used to shape the poking response to the cinnamon scent. Each session consisted of 80 trials in which cinnamon was presented an equal number of times at each of the five locations. Rats remained in this phase until a session was completed in 30 m or less and in which no approximate responses were reinforced by the researcher. Over the following several sessions, rats were trained to make the nose poke response to each of the stimuli that would be used in simple discrimination training. Each session consisted of 70 trials in which a scent was presented at one of the five locations. The stimulus was presented an equal number of times in each location in a pseudo-random order. A trial began with the illumination of all three houselights. When the rat broke the photobeam in front of the nose poke wall, the stimulus scent began to emanate from one of the locations and continued to emanate until the rat poked its nose into that location far enough to break the photo beam. Such responses resulted in the delivery of a pellet from the lighted pellet dispenser. Responses to an uncued location had no consequences. There was a 10 s ITI with the houselights off between each trial. Rats experienced such sessions with each of the six stimuli. In addition, there were also sessions in which the stimuli from a given set were presented together in the same session (e.g., on half the trials, butterscotch was presented and on the other half orange was presented). Sessions were conducted with a given stimulus (or set of stimuli) until 95% of the first responses on a trial were to the location in which the scent was emanating.

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Simple discrimination and reversal training. Following pretraining, all rats were trained on a series of simple discriminations and reversals. Rats were first trained with Set A. Each session consisted of 80 trials in which both scents were simultaneously presented at two of the five locations. A trial began with the illumination of the houselights. Once the rat broke the photobeam in front of the nose poke wall, scents began to emanate from two of the five locations (e.g., butterscotch at location 1 and orange at location 3, etc). Each scent was presented at each location an equal number of times throughout the session in a pseudo-random order. One stimulus (e.g., butterscotch) was designated as correct and responses to it were reinforced on each trial. Rats were given five seconds to consume the pellet, and then a 5 s ITI ensued with the houselights off. The other stimulus (e.g., orange) was designated as incorrect and responses to it ended the trial. Responses to an uncued location were recorded but had no consequences. Nonreinforced trials were separated by a 10 s ITI with the houselights off. Rats remained in training until reaching accuracy criteria of 85% correct or better and at least three sessions. On the session immediately following achievement of the accuracy criteria, the reinforcement contingencies were reversed. For example, if responses to butterscotch had resulted in reinforcement and responses to orange had resulted in the end of trial, responses to orange were now reinforced and responses to butterscotch ended the trial. Rats remained in reversal training until meeting the aforementioned accuracy criteria. When discrimination and reversal training with Set A was completed, rats experienced identical training with Sets B and C. Results On average, rats learned the initial discrimination between the Set A stimuli faster than they did the reversal: training took an average of 6.16 sessions (range: 4 – 10 sessions) and the reversal training took an average of 11.83 sessions (range: 5 – 25 sessions). Initial training on Sets B and C tended to take fewer sessions than training on Set A: for Set B, rats averaged 3.5 sessions to criteria (range: 3 – 4 sessions) and for Set C, rats averaged 4.5 sessions to criteria (range: 2 – 13 sessions). Reversal learning, however, was comparable across all three sets. For Set B, reversal learning took an average of 11 sessions (range: 5 – 25 sessions), whereas for Set C, it took an average of 9.17 sessions (5 – 18). ANOVA indicated that rats took significantly longer to learn the reversal problems than the initial discriminations, F (1,5) = 18.17, p < .007. There were no significant differences in acquisition between stimulus sets, F (2,10) = 0.43, p > .662, nor was there an interaction, F (2,10) = .086, p > .918. Individual acquisition for the initial discrimination and reversal phases are depicted in Figures 2, 3, and 4 for stimulus Sets A, B, and C, respectively. As can be seen from the figures, when initial training began with each stimulus set, accuracy was at chance levels (50% correct) and steadily increased to 85% correct or better. By the end of training, accuracy was 88.75% (range: 86.25% - 92.5%), 88.13% (range: 85% - 96.25%), and 91.94% (range: 86.67% - 96.67%) for Sets A, B, and C, respectively. Moreover, for every rat (except C1 on Set C), on the first reversal session for each stimulus set, accuracy was well below chance: 26.25% (range: 7.5% - 32.5%), 34.79% (range: 23.75% - 42.5%), and 40.83% (range: 25% - 62.5%) for Sets A, B, and C, respectively. Accuracy tended to remain below chance for several sessions before it began to increase to criterion levels.

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Figure 2. Individual subject data for acquisition and reversal for Stimulus Set A. Open circles indicate the initial discrimination and filled circles indicate the reversal.

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PERCENT CORRECT

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Figure 3. Individual subject data for acquisition and reversal for Stimulus Set B. Open circles indicate the initial discrimination and filled circles indicate the reversal.

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Figure 4. Individual subject data for acquisition and reversal for Stimulus Set C. Open circles indicate the initial discrimination and filled circles indicate the reversal.

Error patterns during initial discrimination training and reversal training were also analyzed. Data from the first and last sessions with each set from each phase (initial and reversal training) were compared. For all three stimulus sets, rats tended to make more errors during the first session than during the last session, Fs (1,4) = 382.5, 642.29, and 68.68, p < .05 for Sets A, B, and C, respectively. For Sets A and B, rats also tended to make more errors in reversal training than in initial training, Fs (1, 4) = 55.45 and 19.84, p < .05, respectively, but this was not the case for Set C. Errors were examined also according to proximity of the stimuli during training. Because there were five stimulus locations, stimuli could be presented with a differing number of locations between them across trials. Table 1 indicates the percentage of trials on which errors occurred when stimuli were presented with zero, one, two or three locations between them for each stimulus set. Data are averaged across subjects on the first and last session for each training phase (initial training and reversal training).

TABLE 1, NEXT PAGE

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Table 1. Average subject data indicating where stimuli were located (% trials) when an error was made. Set A

Set B

Set C

First

Last

First

Last

First

Last

Adjacent

41.67

2.60

28.65

5.20

29.69

10.94

1 Away

48.83

9.72

31.25

4.17

25.69

15.28

2 Away

48.96

12.50

38.54

7.29

37.50

18.75

3 Away

45.83

8.33

47.92

31.25

37.50

14.58

Adjacent

76.04

4.69

71.88

9.90

48.96

7.29

1 Away

70.14

10.42

65.28

9.03

43.75

15.28

2 Away

76.04

10.42

55.21

16.67

48.96

11.46

3 Away

70.83

14.58

58.33

14.58

58.33

22.92

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Initial

Reversal

For Set A, there were no differences in the percentage of errors made depending on where the stimuli were presented, F (1,4) = 1.07, p > .39, and there were no interactions with session or training phase, Fs (3,12) = 1.41, .63, and .55, p > .28, .60, and .65. For Set B, there also was no main effect of presentation location, F (1,4) = 3.14, p > .07, but there was an interaction between training phase and presentation location, F (3,12) = 4.58, p < .02. Post-hoc contrasts indicated that in the initial training phase, more errors were made when stimuli were presented with three locations between them than with zero or one location between them (p < .02 and .03, respectively) but that there were no differences during the reversal training phase. Finally, for Set C, there was a main effect of presentation location, F (1,4) = 3.55, p < .05. Post-hoc contrasts indicated that more errors were made when stimuli were presented with three locations between them than when stimuli were presented adjacently. There was also an interaction between training phase and presentation location, F (3,12) = 3.79, p < .05. Post-hoc contrasts indicated that there were no differences in the percentage of errors during initial training but that during reversal training, rats made more errors when the stimuli were presented with three locations between them than when stimuli were presented adjacently or with two locations between them (p < .004 and .03, respectively). In sum, the error pattern data indicate that stimulus presentation location did not influence discrimination accuracy. Rats tended to make the same amount of errors regardless of the proximity of the stimuli. Two exceptions to this were for Set B during initial training and Set C during reversal training. In both of those cases, rats tended to make more errors when the stimuli were presented farther apart.

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Finally, error patterns were examined to determine if rats displayed any consistent position preferences. Specifically, the percentage of errors made when the S+ was presented at each of the five nose poke locations was calculated for each rat during each discrimination and reversal. The data indicate that no clear location preference existed across stimulus location, F (4, 20) = .195, p > .05.

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Discussion The automated olfactory discrimination procedure was effective in producing rapid discrimination learning in all six rats. All rats were able to meet the accuracy criterion of 85% correct for the initial discrimination within 13 sessions. In most cases, the criterion was met in five or fewer sessions. Moreover, learning rates were comparable across all three stimulus sets, indicating that all scents were of similar discriminability. For all rats, reversal learning took longer than did the initial discrimination. In many cases, reversal learning took twice as many sessions. This result replicates results previously found in mice trained to dig in scented sand cups (Mihalick et al, 2000). Previously, Slotnick and Katz (1974) reported evidence of reversal learning set. Rats were trained to make a nose poke response to a positive stimulus and to refrain from responding to a negative stimulus in an apparatus in which all odors were presented in a single location. Rats were trained on a series of 16 discrimination problems, and as training progressed, rats learned each subsequent problem faster than the previous one. By contrast, we did not find evidence of learning set in the current experiment. No differences were found in rate of learning each of the simultaneous discriminations. One reason that we did not find a reversal learning set effect may be that all three original discriminations were learned quickly (there were only four cases in which training of a particular problem took more than 15 sessions). The scents in this study were chosen specifically because it was easy for the researchers to discriminate them from one another (thus, we were able to quickly ensure that the apparatus was working properly). Possibly, a learning set phenomenon can be demonstrated in this paradigm when odors that are more difficult to discriminate are used. Moreover, there were several procedural differences between the two studies. In the Slotnick and Katz study, rats were required to respond in one location and a successive discrimination procedure was used whereas in the current study, a simultaneous discrimination procedure was used. Possibly, a learning set would develop with the specific stimuli used in this study when a successive procedure is employed. Finally, Slotnick and Katz utilized 16 different stimulus sets whereas we only utilized three. The use of a greater number of stimulus sets increases the likelihood of finding differences in the rate of learning over time. The fact that rats were able to quickly acquire the initial and reversal discriminations makes this apparatus ideal for use in behavioral neuroscience. For example, researchers interested in investigating the neural substrates of learning and memory can use this task to illustrate differences between intact rats and those that have experienced damage to particular brain structures. Rats can be trained on the basic task relatively quickly, and the results are easy to interpret. Moreover, automation makes it possible for researchers to test multiple animals at a single time, thereby increasing productivity by decreasing the length of time required to complete a discrimination series. Within the domain of discrimination learning, this apparatus can be modified for additional tasks that involve shifting sensory modalities, such as those conducted by Strupp and colleagues (Garavan, et al., 2000; Hilson & Strupp, 1997). Such extradimensional shift studies could determine how readily rats learn when the discriminative stimulus is shifted from visual to olfactory cues and vice versa. Moreover, the effects of stimulus compounds can be studied. The olfactory control devices allow for the simultaneous presentation of up to three scents in a single location as well as simultaneous presentations of odor and visual cues. This apparatus also has flexibility beyond simple discrimination training. For example, odors can be presented in two or more locations in a concurrent operant procedure in which each location is

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associated with a different reinforcement schedule. Alternatively, tasks could be devised in which rats are required to respond in a particular sequence, similar to what is required in a radial arm maze procedure. Finally, this procedure can be expanded for studies involving conditional stimulus control. For example, rats could be trained on a matching to sample procedure in which odor stimuli are presented in differing locations across trials. Prior work with rats has shown that when trained on matching to sample in which samples and comparisons appear in the same locations across trials, that the effective stimulus is the nominal stimulus (e.g., a flashing light) combined with its location (e.g., a center response key; see Iversen, 1997). Work with pigeons has indicated that when training is conducted with samples and comparisons that change locations across trials, the effective stimulus is more likely to be the nominal stimulus alone (Lionello-DeNolf & Urcuioli, 2000). If such a procedure is successful in training rats on conditional discriminations, their abilities on more complex (and interesting) behavioral problems, such as transitivity and stimulus equivalence, could be assessed. References Bunsey, M., & Eichenbaum, H. (1996). Conservation of hippocampal memory function in rats and humans. Nature, 379, 255-257. Dudchenko, P. A., Wood, E. R., & Eichenbaum, H. (2000). Neurotoxic hippocampal lesions have no effect on odor span and little effect on odor recognition memory, but produce significant impairments on spatial span, recognition and alternation. The Journal of Neuroscience, 20, 2964-2977. Dusek, J. A., & Eichenbaum, H. (1997). The hippocampus and memory for orderly stimulus relations. Psychology, 94, 7109-7114. Garavan, H., Morgan, R. E., Mactutus, C. F., Levitsky, D. A., Booze, R. M., Strupp, B. J. (2000). Prenatal cocaine exposure impairs selective attention: evidence from serial reversal and extradimensional shift tasks. Behavioral Neuroscience, 114, 725-738. Hilson, J. A., Strupp, B. J. (1997). Analyses of response patterns clarify lead effects in olfactory reversal and extradimensional shift tasks: assessment of inhibitory control, associative ability, and memory. Behavioral Neuroscience, 111, 532-542. Iversen, I. H. (1997). Matching-to-sample performance in rats: a case of mistaken identity? Journal of the Experimental Analysis of Behavior, 68, 27-45. Lionello-Denolf. K. M., & Urcuioli, P. J. (2000). Transfer of pigeons’ matching to sample to novel sample locations. Journal of the Experimental Analysis of Behavior, 73, 141-161. Lu, X. M., Slotnick, B. M., & Silberberg, A. M. (1993). Odor matching and odor memory in the rat. Physiology and Behavior, 53, 795-804. McIlvane, W. J., & Cataldo, M. F. (1996). One the clinical relevance of animal models for the study of human mental retardation. Mental Retardation and Developmental Disabilities Research Reviews, 2, 188-196. Mihalick, S.M., Driscoll, L.L. & Strupp, B.J. (July 2001). Development of a cognitive assessment battery for mice. Presented at the meetings of the Society for Neurobehavioral Teratology Society, Montreal, Canada.

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Mihalick, S. M., Langlois, J. C., Krienke, J. D., & Dube, W. V. (2000). An olfactory discrimination procedure for mice. Journal of the Experimental Analysis of Behavior, 73, 305-318. Neill, J. C., & Harrison, J. M. (1987). Auditory discrimination: The Kornorski quality-location effect. Journal of the Experimental Analysis of Behavior, 48, 81-95. Nigrosh, B. J., Slotnick, B. M., & Nevin, J. A. (1975). Olfactory discrimination, reversal learning, and stimulus control in rats. Journal of Comparative and Physiological Psychology, 89, 255-294.

This document is copyrighted by the American Psychological Association or one of its allied publishers. This article is intended solely for the personal use of the individual user and is not to be disseminated broadly.

Pena, T., Pitts, R. C., & Galizio, M. (2006). Identity matching-to-sample with olfactory stimuli in rats. Journal of the Experimental Analysis of Behavior, 85, 203-221. Ramus, S. J., & Eichenbaum, H. (2000). Neural correlates of olfactory recognition memory in the rat orbitofrontal cortex. The Journal of Neuroscience, 20, 8199-8208. Slotnick, B. M., & Katz, H. M. (1974). Olfactory learning-set formation in rats. Science, 185, 796-798. Sidman, M. (1987). Two choices are not enough. Behavior Analysis, 22, 11-18. Wood, E. R., Dudchenko, P. A., & Eichenbaum, H. (1999). The global record of memory in hippocampal neuronal activity. Nature, 397, 613-616.

Author Note This research was supported by National Institute of Mental Health grant R21 MH67801-02 to Karen Lionello-DeNolf. We thank Camila Domeniconi, Cara Marchese, and Kerrilynn Lacerte for their assistance in data collection. We also thank William McIlvane for his comments on an earlier version of the manuscript. Sheila Mihalick is now at STRATTUS, the Mental Health Centre of TILL (Toward Independent Living and Learning, Inc.), Dedham, MA

Author Contact Information: Karen Lionello-DeNolf 9 Bylund Ave. Auburn, MA 01501 E-Mail: [email protected] Sheila Mihalick 7 Sherman Street 2BE, Charlestown, MA 02129 E-Mail: [email protected].

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