Journal of Neuroscience Methods, 44 (1992) 197-207

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© 1992 Elsevier Science Publishers B.V. All rights reserved 0165-0270/92/$05.00

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Production of a serial position effect in rats using a 12-arm radial maze David N. Harper, John C. Dalrymple-Alford and A n t h o n y P. M c L e a n Department of Psychology, University of Canterbury, Christchurch (New Zealand) (Received 27 March 1992) (Revised version received 13 July 1992) (Accepted 22 July 1992)

Key words: Radial-arm maze; Memory; Serial position effect; Primacy; Recency; Serial probe recognition; (Rats) T h e effects of item position (the serial position effect: SPE) on the recognition of a list of arms presented in an 8 - a r m radial maze have not been shown to be robust across studies which differ in numbers of subjects, amount of training and task difficulty. The present study examined whether more robust SPEs could be obtained in rats with a 12-arm radial maze using a matching-to-sample serial probe recognition (SPR) procedure. In Part 1, 23 rats received extensive training on recognition of list of arms from a 5-arm list and, in Part 2, 20 rats received training with a 7-arm list. Both Parts 1 and 2 showed that a reliable and persistent SPE emerged due to superior recognition of items at the first and last serial positions compared with the middle positions. However, the SPE was more pronounced with the 7-arm than 5-arm list. It is argued that adequate task difficulty along with sufficient subject and trial n u m b e r s is necessary to produce a clear SPE. In Part 3, an alternative m e a n s of assessing accuracy derived from signal-detection theory is examined, and the procedural requirements for its use are identified. Although this measure did not alter the conclusions reached using percent correct, it is proposed that the bias-free measure, log d, is superior to traditional indices of memory performance which may obscure the presence of, or changes in, the SPE. The procedures used here provide a valuable m e a n s to produce clear, reliable and persitent SPEs. Such procedures are essential if researchers are to be confident about the effects of lesions or drugs upon list memory in their attempts to explore the neurological bases of memory and model h u m a n neurological disorders.

Introduction

The equivalence of animal and human memory is a main area of interest in the neurosciences (e.g., Wright and Watkins, 1987; Reed et al., 1991). The development of procedures to test animal memory is of particular relevance when examining animal models of human neurological

Correspondence: David N. Harper, D e p a r t m e n t of Psychology, University of Canterbury, Private Bag, Christchurch, New Zealand. Tel.: (03) 3667-001 (ext. 7174); FAX: (03) 642-181.

disorders. An important phenomenon in humans is that, when they are given a list of items to remember, recall is best for items presented early in the list (primacy effect) and late in the list (recency effect) with inferior performance on items from the middle of the list. This pattern, called the serial position effect (SPE), is altered in people suffering neurodegenerative disorders such as Alzheimer's disease, Huntington's disease and alcoholic Korsakoff syndrome (e.g., Kesner, 1988a,b; Delis et al., 1991). A number of studies have attempted to demonstrate an SPE in animals (e.g., DiMattia and Kesner, 1988; Kesner

198 and Beers, 1988; Kesner et al., 1988), but the interpretation of their findings is compromised by the absence of clear and robust SPEs in intact or lesioned animals. The most common animal used to model neurodegenerative disorders is the rat. Attempts to demonstrate the presence of both primacy and recency in rats have usually examined memory for lists of arms presented in an 8-arm radial maze. Memory for a list of arms is tested using the serial probe recognition (SPR) procedure. Typically, an SPR trial consists of two phases: a presentation phase in which a list of items is presented, and a test phase in which recognition for a single item from the list is examined. While the recency effect is often obtained in the radial maze version of an SPR procedure, there has been difficulty in demonstrating a primacy effect. Roberts and Smythe (1979) presented sequences of 1, 3, 5 or 7 arms before testing recognition. They found that, irrespective of the list length used, recognition was worse for the 1st and best for the last items in the list. That is, they found clear evidence of a recency but not a primacy effect. Bolhuis and van Kampen (1988) found that at 30-s delay between presentation and recognition there was a recency but not primacy effect. However, a weak primacy effect emerged at 60-min delay due to accuracy decreasing more dramatically for late items in the list compared with earlier ones. While some studies have not been able to demonstrate a clear SPE, others have had more success. DiMattia and Kesner (1984) gave rats a 5-arm list in a standard 8-arm maze and compared performance when the correct choice was either to return to a previously presented arm (matching to sample) or to enter the novel arm (non-matching to sample). When the task required non-matching to sample, a clear recency effect was observed, but primacy was not evident. However, both primacy and recency effects were clearly evident when the task involved matching to sample. The failure of Roberts and Smythe (1979) and Bolhuis and van Kampen (1988) to observe primacy may have been due to their requiring the rat to non-match to sample. However, the rule governing the test phase is not the

only aspect of the task which may determine the presence or absence of primacy effects. Recently, Reed et al. (1991) demonstrated both primacy and recency in 8 of 11 rats when they were presented with a list of 5 non-spatial items and were required to non-match to sample. Furthermore, some studies conducted by Kesner and colleagues have failed to replicate the strong SPE observed by DiMattia and Kesner (1984), despite similar methodologies. For example, Kesner et al. (1988) examined the effect of various brain lesions on SPR performance using the matching rule and a list of 5 arms presented in an 8-arm maze. Prior to surgery, 4 of 5 subject groups did not show an SPE with primacy or recency evident. Other lesion studies have also found either no evidence of an SPE in prelesion or control animals (e.g., DiMattia and Kesner, 1988; Kesner and Beers, 1988) or only weak SPEs (e.g., Kesner and Holbrook, 1987; Kesner et al., 1989) compared to data obtained by DiMattia and Kesner (1984). Consequently, the apparent effect of lesions on primacy and recency in these studies is not convincing as these 2 features of the SPE were not evident prior to surgery or in control animals. The problem in obtaining consistent SPEs means that researchers cannot be confident about the effect of their experimental manipulations. Thus more detailed investigation of the basic SPR procedure is needed to determine which conditions establish clear, reliable and persistent SPEs. The various studies that have investigated the SPE in rats have used tasks of differing degrees of difficulty, different group sizes and amounts of training. These aspects of the SPR procedure may contribute to inconsistencies observed, and the present study examines conditions which may influence the emergence, reliability and persistence of an SPE in a radial maze. One aspect of the SPR task that may be vital for the emergence of an SPE is task difficulty. DiMattia and Kesner (1984) suggested that the reason both primacy and recency emerged with a matching rule (rather than non-matching to sample) is that rats found this task more 'effortful' and therefore processed the stimuli more deeply. In their study rats took longer to learn the match-

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ing than the non-matching rule, indicating that matching was more difficult. Although Reed et al. (1991) used a non-matching rule, they noted that their task, which used non-spatial items, was more difficult for rats to learn than corresponding radial maze versions. Again primacy and recency may have emerged due to more effortful processing being required. In the present study, we sought to achieve high task difficulty, thereby increasing the chance of observing an SPE by using a 12-arm rather than 8-arm maze used in previous research. A list of 5 arms presented in a 12-arm maze demands more of a rat's ability to discriminate a novel from a familiar arm. In an 8-arm maze adjacent arms are separated by 45 °, whereas in a 12-arm maze the difference between arms is 30 °. Hence, in a 12arm rather than 8-arm maze there is less of a spatial differentiation between arms, resulting in greater similarity between them. In Part 1 of the present study 5-arm lists were presented to rats in a 12-arm maze, and the rats' ability to return to a previously visited arm was examined. A 2nd, and potentially valuable, means of increasing the difficulty of the SPR task is to increase task demands by increasing the list length. As most studies have used an 8-arm maze to examine list learning in rats, the typical list length has been 5 items long. To extend the list further in an 8-arm maze is problematic as it is necessary to keep some arms unvisited in the presentation phase to be used as novel arms in the test phase. If the list length were extended too far in the 8-arm maze it would become easier for the rat to r e m e m b e r unvisited arms which thereby lessens the load on memory. With 12 arms from which to draw, the list length can easily be extended to 7 arms, still leaving 5 arms unvisited. In Part 2 of the present study the list length was increased from 5 to 7 arms to assess whether SPE is more pronounced with this increase in task difficulty. One particular benefit of the 12-arm maze is that all 5 (Part 1) or 7 (Part 2) members of the presentation list can be tested in 1 day, using different non-visited arms on each test trial. Another issue that needs clarification is why some studies using similar methodologies are inconsistent with one another in the emergence of

a clear SPE (e.g., DiMattia and Kesner, 1984, 1988; Kesner and Beers, 1988; Kesner et al., 1988). These studies varied in the number of subjects used a n d / o r the amount of training received so these aspects may be important in the emergence and maintenance of a clear SPE. DiMattia and Kesner (1984) had a larger group size (n = 10) than did the other studies (n = 4-6) so perhaps the presence of an SPE depends on relatively high subject numbers. The influence of amount of training may be less clear; some studies (e.g., Kesner and Beers, 1988; Kesner et al., 1988) have used fewer training trials while other studies (e.g., DiMattia and Kesner, 1988) have given more, compared to DiMattia and Kesner (1984). Thus the effects of subject numbers and amount of training needed to be investigated in more detail as was done in the present study. Part 1 examined performance in 23 rats over 30 sessions (150 trials) to assess if extended training altered the maintenance of an SPE obtained using a 5-arm list in a 12-arm maze. Part 2 examined not only group performance of a relatively large number of subjects (20) and trials (70) but also individual performances with the 7-arm list to assess whether an SPE obtained from a g r o u p average is reflected in individual rats. If few subjects show individual SPEs, then low subject numbers will be less likely to reveal an SPE when they are grouped together. Reed et al. (1991) found that 8 of 11 individual rats showed an SPE using an object-recognition task. However, given that most SPR research with rats is done with a radial-arm maze, it is important to determine whether individuals demonstrate both primacy and recency in this maze task. Finally, the usual measure of performance in the SPR procedure, i.e., percent correct, has 2 problems. First, percent correct does not allow for the effect that response bias may have on accuracy. For example, a rat may choose an arm due to a preference that has nothing to do with memory for that arm (e.g., a 'desirable' location). Second, percent correct is on a non-infinite scale and may obscure subtle differences in performance at high or low overall accuracy (e.g., Kesner et al., 1988). Thus, percent correct may produce difficulties in interpretation when task difficulty

200 is low or group sizes are small. Recognition can instead be examined using measures derived from signal-detection theory (e.g., Davison and Tustin, 1978). Two important measures are 'log d ' which is a measure of correct choices or discriminability when response bias has been eliminated and 'log b' which is a separate measure of that response bias. As log d removes the confounding influence of response bias and has an infinite scale, it has the potential to be a measure of accuracy superior to percent correct. Some researchers investigating the neurological basis of memory have already employed either these measures (e.g., Kirk et al., 1988) or similar measures derived from signal-detection theory (e.g., Aggelton et al., 1991). In Part 3 of the present study, we describe procedures that enable the use of these signal-detection measures to examine SPR performance in the 12-arm radial maze.

Method

Subjects Twenty-three naive male Wistar rats approximately 4 months old at the start of the experiment were used in Part 1 of the experiment; 20 of these rats were used in Parts 2 and 3. The rats were housed 4 / c a g e and were maintained at 8 0 85% of their ad libitum body weight with free access to water throughout the study.

Apparatus The apparatus was an elevated (85 cm from the floor) radial maze, comprising 12 evenly spaced aluminium arms radiating from a central wooden platform (35 cm wide, painted black). Each arm (9 cm wide, 65 cm long) was constructed with 3-cm borders, a 25-cm-high perspex barrier at the proximal end, and a 2-cm-diameter food well drilled in a wooden block placed at the distal end. Access to each arm was controlled via a clear plastic guillotine door located between the platform and arm. Doors could be raised singly or in combination by means of pulleys operated by the experimenter adjacent to the maze. The windowless room housing the maze was lit by two 22-W fluorescent lamps. A door, shelves and table

provided ample external cues to the maze, the position of which was kept constant.

Procedure For an initial pretraining session, groups of rats were able to explore freely the entire maze with chocolate chips (0.1 g) scattered over the length of all the arms. For the next 2 sessions, chocolate chips were available only at the end of each arm. For the next 3 pretraining sessions (with 3 trials/session) an individual rat was placed on the central platform and a randomly chosen door was lifted, allowing access to 3 pieces of chocolate at the end of the arm. Performance in the matching-to-sample SPR task was then shaped using progressively longer lists of arms. For each of 5 sessions (with 3 trials/session), rats were presented with a single arm in the presentation phase prior to the test phase. In the following 7 sessions (with 3 trials/session), rats were presented with a 3-arm list in the presentation phase prior to the test phase. Finally, the experiment proper began with a 5-arm list presented in Part 1, followed by a 7-arm list in Parts 2 and 3. Irrespective of list length, the task involved 2 phases: a presentation phase in which a sequence of arms was successively available to the subject followed by a test phase in which recognition for 1 of the list arms was examined. At the start of a trial, a rat was placed on the central platform and all doors were lowered. A predetermined sequence of arms was then presented to the rat, 1 arm at a time. The door to the 1st arm in the sequence was raised, allowing the rat to run down the arm and gain a single piece of chocolate. When the rat returned to the central platform the door was lowered and the door to the next arm in the list was raised. After all arms in the list sequence had been visited, 1 of those arms was then rebaited with 3 pieces of chocolate before the experimenter simultaneously raised the door to the rebaited arm and the door to an unbaited arm not visited in the previous list. The interval between the last door being lowered in the presentation phase and 2 doors being raised in the test phase ranged from 4 to 8 s. In the test phase the rat was required to return to the 1 arm of the

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pair which had been visited during the presentation phase. Once 3 paws had entered an arm, the door was lowered and the rat was counted as having m a d e a response. Sequences were chosen that did not allow for a response strategy to aid recognition of the previously presented arm (e.g., lists of arms 1, 3, 5, 7, 9 or 1, 2, 3, 4, 5 were not allowed). Comparison (previously unvisited) arms chosen for each test phase of a trial were always next door but one to the correct arm; on 50% of the trials the comparison arm was to the right of the correct arm and on the other 50% it was to the left. Sessions were run 5 days a week. In any session a rat was exposed to only 1 sequence, repeated for all trials in that session. In Part 1, rats were tested for 5 trials/session. On each trial, the 5 list arms were presented and then recognition was tested for 1 of those arms. To allow all serial positions in the list to be tested once (for each rat in a given session), on each trial a different list arm and 1 of 7 non-list arms were tested for recognition. The order of testing serial positions was varied across rats/session and within rats over sessions. After being run on a trial, the rat was removed from the apparatus and the next rat was run, until all rats had received 1

trial. The 1st rat was then run on the 2nd trial of the session and so on until all rats had completed their 5 trials for the day. The rats were trained for 30 sessions in Part 1 (i.e., 150 t r i a l s / r a t across all serial positions). In Part 2 rats were again tested for 5 trials/session. The list length in the presentation phase was extended to 7 arms, but only 5 positions in the 7-arm list were tested for recognition (serial positions 1, 3, 4, 5, and 7). Otherwise the procedure was the same as in Part 1. The rats received 15 sessions of training in Part 2 (i.e., 75 t r i a l s / r a t across all serial positions). Parts 1 and 2 measured accuracy with percent correct; Part 3 measured accuracy with the biasfree measure of log d derived from signal-detection theory (Davison and Tustin, 1978). Part 3 lasted for 6 sessions of training and tested the same serial positions as Part 2 but used 6 'new' sequences of 7-arm lists (see Table I). These new sequences were generated under the same rules that governed production of earlier lists but, in addition, had to be capable of allowing a bias-free measure of discriminablity (log d) between arm pairs. In this procedure each arm had to be presented with only 1 other arm. In one-half of the trials (involving that stimulus

TABLE I SIX S E Q U E N C E S U S E D IN P A R T 3 Each n u m b e r represents an arm on the maze. All 12 arms are used but only arms 1, 3, 5, 7, 9 and 11 appear in positions 1, 4, and 7 and only arms 2, 4, 6, 8, 10, and 12 appear in positions 2, 3, 5, and 6. Hence, positions 1, 4, and 7 are comparable in that the same arms are presented in each. T h e same is true for positions 3 and 5. N u m b e r s in brackets are the comparison arms shown with the list arm during the test phase. Positions 2 and 6 have no comparison arm because they were not tested. Sequence

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pair) 1 of the arms was presented in the list and the other arm was not; when tested for recognition, both arms in the pair were presented simultaneously and the rat chose between them. On the other half of the trials (involving the stimulus pair), the alternate arm in the pair was presented in the list. Such pairing of arms makes it possible to generate the stimulus-response matrix in Fig. 1 which allows for calculation of indices for recogniziability (log d) and response bias (log b). From this matrix the following calculations can be made: log d = 0.5 log ( P w P z / P x P y )

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Eqn. 1 provides a measure of discriminability that is free from the influence of response bias. Eqn. 2 is a measure of that response bias (see Davison and Tustin, 1978; McCarthy and Davison, 1981, 1984 for examples of how these equations are derived).

Fig. 2. Percent correct according to serial position in a list of 5 arms in a 12-arm radial maze. The 5 points on the horizontal axis represent serial positions 1-5, respectively. Five blocks of 6-day sessions are shown. The measure of percent correct was gained by averaging over all subjects across the 6 sessions in a block for a given serial position. Error bars were obtained from the mean squared error of each score.

Results

serial position on performance ( F (4, 8 8 ) < 1.0) during sessions 1-6. By sessions 7-12, a serialposition curve emerged, due to accuracy at positions 1,2 and 5 being generally greater than at positions 3 and 4. That is, both a primacy and recency effect were evident. An analysis of sessions 7-12 revealed that there was a main effect of serial position ( F (4, 8 8 ) = 8.15, P < 0.05). Planned comparisons revealed that positions 1,2,3 and 5 were all significantly different from position 4 at P < 0.05. The only other significant difference at this level was between positions 1 and 3. Inferior performance in positions 3 and 4 relative to positions 1,2 and 5 persisted through the 3 subsequent blocks of training, and a serialposition effect was still clearly evident in sessions 25-30 ( F (4, 88) = 2.96, P < 0.05). Planned comparisons for this block showed that positions 1,2 and 5 were all significantly different from position 4 at P < 0.05. Even though position 4 was consistently inferior to all the other positions (except to position 3 in sessions 19-24), as training progressed accuracy at position 4 increased from 56% in sessions 1-6 to 70% in sessions 25-30; however, accuracy at the 2 extremes (posi-

Of interest in Part 1 was whether an SPE, with both primacy and recency present, could be obtained with a 5-arm list in a 12-arm radial maze and the effect maintained over training sessions. Fig. 2 shows 5 consecutive blocks of sessions in which percent accuracy in the recognition test is given for each serial position. Each data point represents the average score of 23 rats from 6 sessions of training. In sessions 1-6, accuracy lay between 60 and 70%, irrespective of serial position. A 1-way A N O V A with serial position as a repeated measure showed that there was no main effect of

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Fig. I. The stimulus-response matrix for a ' y e s - n o ' detection test. Only when the response is correct does the animal gain reinforcement. W, X, Y, and Z are tallies of the number of events in each cell.

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tions 1 and 5) remained fairly stable once the SPE was established. Part 2 of the experiment extended the list length from 5 to 7 items. The first 3 days of training (sessions 31-33) with the new list length were counted as a period of familiarisation and were not included in the analysis. Fig. 3 shows accuracy in recognition according to serial position with the new list length. From the 12 sessions of training in Part 2, 2 blocks of data were obtained. Each data point represents the average percent correct of all 20 rats over 6 sessions of training. For both blocks, accuracy in the middle 3 positions (3, 4 and 5) was below that of both the 1st and last positions (1 and 7). A 1-way A N O V A with serial position as a repeated measure revealed that there was a main effect present for sessions 34-39 ( F (4, 76) = 5.03, P < 0.05) and sessions 40-45 ( F (4, 7 6 ) = 6.73, P < 0.05). Planned comparisons for sessions 34-39 revealed that position 1 was significantly different from 4 and 5 and that position 7 was significantly different from 3, 4, and 5 at P < 0.05. Planned comparisons for sessions 40-45 revealed even stronger support for a serial-position curve with both primacy and recency present. Positions 1 and 7 were not significantly different from each other but were both significantly different from positions 3, 4 and 5 at P < 0.05.

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Production of a serial position effect in rats using a 12-arm radial maze.

The effects of item position (the serial position effect: SPE) on the recognition of a list of arms presented in an 8-arm radial maze have not been sh...
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