Learning and Motivation 53 (2016) 1–6

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Learning and Motivation

journal homepage: www.elsevier.com/locate/l&m

The effects of differential outcomes on learning and memory

in young and aged rats
L. Rebeca Mateos a,∗ , Kenneth Madrigal b , Carlos Flores b , J. Bruce Overmier c
a
Instituto de Gestión del Conocimiento y el Aprendizaje en Ambientes Virtuales, Universidad de Guadalajara, Avenida la Paz 2453, Arcos
Sur, Guadalajara, Jal. 44140, Mexico
b
Centro de Estudios e Investigaciones en Comportamiento, Universidad de Guadalajara, Fco. De Quevedo 180, Arcos Vallarta,
Guadalajara, Jal. 44130, Mexico
c
Department of Psychology, University of Minnesota, 75 E. River Rd., Minneapolis, MN 55455, USA

a r t i c l e i n f o a b s t r a c t

Article history: It is claimed that using a differential outcomes procedure (DOP) generally results in (1) a
Received 18 July 2015 faster acquisition of discrimination and (2) less disruption in accuracy when a delay interval
Received in revised form 21 October 2015 is inserted between the stimulus cue and the opportunity to respond; this effect is best
Accepted 23 October 2015
known as the differential outcomes effect (DOE). The DOE has been especially evident in
aged participants. However, when acquisition in a matching-to-position task under DOP
Keywords: was compared to that under a non-differential outcomes procedure (NDO) by Savage, Pitkin,
Differential outcomes
and Careri (1999), no difference in rate of acquisition was found between young and old
Conditional discrimination
rats. In the present experiment, we evaluated the effect of using a differential outcomes
Learning
Memory procedure on both learning and memory in young (3 months) and aged (24 months) rats
Young and aged rats in a more standard two-choice stimulus discrimination task. The results reported in this
article showed in both young and aged subjects that DOP led to faster acquisition and less
disruption in the percentage of correct responses as the delay interval was lengthened.
These results confirm that employing DOP is an effective training strategy that can increase
speed of acquisition and enhance memory in both young and aged subjects, with larger
effects being seen in older rats.
© 2015 Elsevier Inc. All rights reserved.

1. Introduction

It is known that age is a factor related to memory deficit (Kubanis & Zornetzer, 1981; Morris & Kopelman, 1986). For
example, in conditional choice tasks, some studies have reported that aged rats show a greater loss of correct responses
compared to younger rats when a delay interval between a stimulus and the opportunity to respond is lengthened (Dunnett,
Evenden, & Iversen, 1988; Dunnett, Martel, & Iversen, 1990).
The usual laboratory procedure for training conditional discriminative choice tasks, called the common outcomes (CO)
consists in reinforcing each correct response (R1 and R2) with the same outcome (O1). Another procedure is non-differential
outcomes (NDO); in this task two different outcomes are presented randomly after a correct response. The Differential
Outcomes Procedure (DOP) basically consists of reinforcing a response (R1), in the presence of a stimulus (S1), with a

∗ Corresponding author.
E-mail address: rebeca.mateos@suv.udg.mx (L.R. Mateos).

http://dx.doi.org/10.1016/j.lmot.2015.10.004
0023-9690/© 2015 Elsevier Inc. All rights reserved.
2 L.R. Mateos et al. / Learning and Motivation 53 (2016) 1–6

specific outcome (O1), and reinforcing a second response (R2), in the presence of another stimulus (S2), with a different
specific outcome (O2).
It has been reported that the decrement in the percentage of correct responses caused by a delay between a stimulus and
the opportunity to respond can be reduced by using the DOP. Also it has been reported that DOP may facilitate learning;
subjects trained with DOP require fewer sessions to reach higher levels of correct responses compared to a NDO procedure
(Peterson, Linwick, & Overmier, 1987; Trapold, 1970; Trapold & Overmier, 1972).
Faster acquisition in discrimination and higher levels of correct responses in memory tasks produced by DOP have been
named the differential outcomes effect (DOE). The DOE has been explained by suggesting that each stimulus (S1 and S2)
comes to evoke a specific outcome expectancy (O1 and O2), and that those expectancies have stimulus properties that
exert control over choice behavior (Chatlosh & Wasserman, 1992; Holden & Overmier, 2014; Linwick, Overmier, Peterson,
& Mertens, 1988; Peterson, Linwick, & Overmier, 1987; Trapold, 1970; Trapold & Overmier, 1972). Alternatively, it has
been suggested that the NDO and the DOP activate different brain systems (Savage, 2001). In any case, note that there are
two things being labelled the DOE, one an effect on acquisition (rate or asymptote) and the other an effect on asymptotic
performance under challenge (e.g., a delay between stimulus and the opportunity to respond).
A DOE has been consistently observed across different species and using different tasks (for reviews see Goeters, Blakely, &
Poling, 1992; Mok, Estevez, & Overmier, 2010; Urcuioli, 2005). The most commonly used tasks have been delayed matching-
to-sample (DMTS), and delayed matching to position (DMTP). The DMTS task consists in the presentation, on each trial,
of one of two possible stimuli (called sample stimuli); after a delay without the sample stimulus, two comparison stimuli
are presented. A response to each comparison stimulus is the correct response following one sample stimulus and not the
other. The DMTP task involves presentation of one of two retractable levers to provide a sample. An animal must then choose
between the levers (make a position response) after a delay (Dunnett et al., 1988, 1990; Ramos & Savage, 2003; Savage, 2001).
Several studies have described the contribution made by the DOP in learning and memory in both human and non-human
animals (e.g., Hochhalter, Sweeney, Bakke, Holub, & Overmier, 2000; Hochhalter & Joseph, 2001; Martínez et al., 2012; Plaza,
Antúnez, Estévez, López-Crespo, & Fuentes, 2012; Plaza, Estévez, López-Crespo, & Fuentes, 2011; Savage, 2001; Savage &
Langlais, 1995; Savage, Pitkin, & Careri, 1999).
There has been one notable exception to this summary. Savage et al. (1999) trained young rats (3 months old) and aged rats
(23 months old) in a matching-to-position (MTP) task. One group of young rats and another group of aged rats were trained
using differential outcomes (DOP), whereas other two groups (young and aged) were trained using non-differential outcomes
(NDO) and then tested with a DMTP. No differences between DOP and NDO groups were observed in the acquisition phase;
all groups met the acquisition criterion at the same time (12 sessions). This result is not consistent with the vast number
of studies which have reported faster acquisition in subjects trained with DOP (e.g., DeLong & Wasserman, 1981; Urcuioli,
1990, 2005; Goeters et al., 1992). However, during the DMTP phase, they did find a clear beneficial effect of using differential
outcomes. The groups trained with a DOP showed less disruption in the percentage of correct responses when a delay was
imposed between the cue and the opportunity to respond than did groups trained with NDO. Additionally, they did not find
differences in accuracy between the young and aged rats trained with delayed DOP. In contrast, subjects trained with NDO
showed a dramatic decrease in the percentage of correct responses in the aged rats as well as a less dramatic decrease in
the young rats as the delay interval was lengthened.
The results of this study are interesting because they reveal that DOP training, especially in aged rats, enhanced memory-
based asymptotic DMTP performance relative to NDO. However, the lack of differences in the initial learning speed could be
a result related to the type of task used (MTP). That is, in a MTP task used by Savage et al. (1999), the sample was exposure
to a spatial location and the response was made to that same spatial location.
Based on the above, it is possible that the task used by Savage et al. (1999) represents a lower degree of difficulty for
the rats resulting in a ceiling effect that does not allow observation of the contribution that the DO training has to learning
speed. To evaluate this possibility, the present study was designed with the purpose of assessing the contribution that the
DO in a two-choice conditional discrimination MTS-type task in young (3 months) and aged (24 months old) rats.

2. Method

2.1. Subjects

The subjects were 32 male experimentally naive Wistar rats; 16 rats were 3 months old (young rats) while the other 16
rats were 24 months old (aged rats) at the start of the experiment. All rats were food deprived and maintained at 80% of
their initial body weights, individually housed and had free water access in their home cages.

2.2. Apparatus and procedure

The apparatus consisted of eight operant test chambers (Med Associates Inc., ENV-008) equipped with a food dispenser
(Med Associates Inc., ENV-203M-45), a water dispenser (Med Associates Inc., ENV-202RM), and two retractable levers (Med
Associates Inc., ENV-112CM) separated by 12 cm, one on each side of the food dispenser: each lever required a 0.25 N force
to be activated. On the wall opposite to the levers and the feeder panel was a general lighting lamp of 28-V. A white noise
amplifier (Med Associates Inc., ENV-225SM) and a speaker were used to produce a sound at 80 dB of 2000 Hz as a conditional
 L.R. Mateos et al. / Learning and Motivation 53 (2016) 1–6 3

60

50

Sessions to criterion
40

30

20

10

0
A-DO A-NDO Y-DO Y-NDO

GROUPS
Fig. 1. Number of sessions to criterion in each group. Values shown are means (bars) and standard errors of the mean (vertical lines). Aged differential
outcomes (A-DO), young differential outcomes (Y-DO), aged non-differential outcomes (A-NDO), and young non-differential outcomes (Y-NDO).

cue. Each chamber was enclosed in a sound-attenuating box (Med Associates Inc., ENV-022MD) equipped with a ventilation
fan that provided sound masking. A computer coupled to an interface (Med Associates Inc., SG-6080D) and the MED-PC IV
software controlled the experimental events and collected data.

2.3. Pre-training

All subjects had two 30 min habituation sessions in the experimental chambers. A fixed time 60 s (FT 60 s) was used
in which 0.1 cc of a 20% sucrose solution or a 45 mg food pellet was randomly delivered. Then, they were exposed to two
sessions of lever press training to both levers.
During these sessions, one of the two levers was randomly extended for 20 s; a lever press was followed by the delivery
of a food pellet or a 0.1 cc solution and retraction of the lever. Every session consisted in the presentation of 50 trials with
the right lever intermixed with 50 trials with the left lever and a 45-s intertrial interval.

2.4. Discrimination (training)

The subjects were assigned to one of two outcomes conditions (DO vs. NDO). On the DO condition two groups were
formed, a young rats group (Y-DO; n = 8) and an aged rats group (A-DO; n = 8). Another two groups were formed for the
NDO condition, a young rats group (Y-NDO; n = 8) and an aged rats group (A-NDO; n = 8). Groups trained in the DO condition
received one 45 mg food pellet upon pressing the right lever if a continuous tone was previously presented or 0.1 cc of
sucrose solution upon pressing the left lever if an intermittent tone was previously presented (correct responses). Subjects
exposed to the NDO condition received random pellet or sucrose presentations upon pressing the correct lever.
Every training session consisted of 60 trials, each discrimination trial started with a 5 s presentation of a continuous
tone or an intermittent tone (0.5-s on-off intervals). Immediately after the presentation of either of the tones both levers
were inserted for 10 s. If the subject emitted a correct response, both levers were retracted, and the scheduled outcome was
presented dependent upon the assigned group (DO or NDO). A 45-s intertrial interval began after a correct response, an
incorrect response, or a failure to respond during the 10-s lever presentation. Training concluded once the subjects reached
a criterion of 90% correct responses for three consecutive sessions.
Once the subjects met the criterion, a retention interval (delay) was added between the tone and insertion of both levers.
The delays were introduced successively at 2, 4, and 8 s, and each delay was in force for three sessions.

3. Results

The mean number of sessions required by the subjects to reach the acquisition criterion (90% correct responses on three
consecutive sessions) is shown on Fig. 1. A two-way ANOVA (age × condition) revealed a main effect of age (young vs. aged
rats), F(1, 28) = 95.738, p < 0.001; aged rats required more sessions (37.50) than the young rats (22.37) to met the acquisition
4 L.R. Mateos et al. / Learning and Motivation 53 (2016) 1–6

100

90

Percent correct
80

70

60

A-DO
A-NDO
50 Y-DO
Y-NDO

40
0 2 4 8
Delay (sec)
Fig. 2. Percent of correct responses for each group as a function of delay. Values shown are means and standard errors of the mean (vertical lines). Aged
differential outcomes (A-DO), young differential outcomes (Y-DO), aged non-differential outcomes (A-NDO), and young non-differential outcomes (Y-NDO).

criterion. Also, a main effect of outcome condition (differential vs. no differential) was found, F(1, 28) = 151.07, p < 0.001;
subjects trained with differential outcomes required 20.43 sessions, whereas subjects trained with non-differential outcomes
required 39.43 sessions. The interaction age × outcome condition was significant, F(1, 28) = 39.783, p < 0.001. To analyze the
interaction, we performed two simple ANOVAs comparing the number of sessions to reach the criterion for young and aged
rats in each outcome condition training (differential vs. non-differential). Aged rats required more sessions (23.12) than the
young rats (17.75), F(1, 14) = 16.11, p < 0.001, in the differential outcomes condition. Also, this effect was found in the non-
differential outcome condition, F(1, 14) = 79–68, p < 0.001; aged rats required 51.87 sessions, whereas young rats required
27 sessions to reach 90% correct responses.
The percentage of correct responses (accuracy) for each group at each delay is presented in Fig. 2. The delay disrupted
conditional discriminative choice performances as shown by the percentage of correct responses. The largest decrease in
accuracy across delays was observed in group A-NDO and the least decrease was observed in Y-DO group, intermediate
decreases in percentage of correct responses were found in Y-NDO and A-DO groups. The mean of correct responses for the
A-DO Group was higher (82%) than the A-NDO group (68%). In the same manner, higher percentage was found in the Y-DO
group (89%) than in the Y-NDO group (81%).
The data were further analyzed using a mixed ANOVA with delay (0, 2, 4, and 8-s) as the within-subject factor and
condition of reinforcement (differential outcomes, non-differential outcomes) and age (young, aged) as between-subjects
factors.
The analysis indicated that there was a main significant effect of delay F(3, 92) = 641.42, p < 0.001. The delay × age interac-
tion was significant, F(3, 92) = 69.63, p < 0.001), also the delay × outcome condition was significant, F(3, 92) = 34.71, p < 0.001).
The triple interaction delay × age × outcome condition also was significant, F(3, 92) = 7.57, p < 0.001). In order to analyze the
triple interaction, we performed two separate ANOVAs, one for each outcome condition (differential and non-differential),
with delay interval (0, 2, 4 and 8-s) as a within factor and age (young vs. aged rats) as a between factor. In both outcomes
conditions, the delay × age interactions were significant; F(3, 138) = 24.34, p < 0.001 for the differential outcome condition;
and F(3, 138) = 56.29, p < 0.001, for the non-differential outcome condition. To analyze differences in the percentage of cor-
rect responses at each delay interval, we performed four one-way ANOVAs for each outcome condition. In the differential
outcome condition, the percentage of correct responses showed significant differences, being higher for young rats than the
aged rats at all delay intervals, 2-s delay (Y-DO = 91%, A-DO = 88%), F(1, 46) = 15.38, p < 0.001, 4-s (Y-DO = 87%, A-DO = 78%), F(1,
46) = 40.57, p < 0.001, 8-s (Y-DO = 78%, A-DO = 62%) F(1, 46) = 44.68, p < 0.001, except the 0-s delay (Y-DO = 92%, A-DO = 92%),
F(1, 46) = 1.44, p = 0.235. In the non-differential outcome condition, we also found differences in the percentages of cor-
rect responses between the young and aged rats, 2-s delay (Y-NDO = 90%, A-NDO = 75%), F(1, 46) = 132.80, p < 0.001, 4-s
(Y-NDO = 80%, A-NDO = 59%), F(1, 46) = 133.75, p < 0.001, 8-s (Y-NDO = 68%, A-NDO = 48%), F(1, 46) = 144.40, p < 0.001, except
during 0-s (Y-NDO = 92%, A-NDO = 91%), F(1, 46) = 0.89, p = 0.351. The absence of an effect at the 0-s delay reflects the fact
that rats were trained to a 90% criterion under this condition.
 L.R. Mateos et al. / Learning and Motivation 53 (2016) 1–6 5

4. Discussion

Generally speaking, both young and old rats trained using a differential outcomes procedure (DOP) required fewer training
sessions to reach the established acquisition criterion, than comparable rats receiving the more standard NDO training. Aged
rats using the “standard” procedures (A-NDO) required the highest number of training sessions to reach the criterion. These
results are consistent with previous studies that have reported enhanced acquisition using DOP during training in other
species (Chatlosh & Wasserman, 1992; Urcuioli, 1990, 2005; Goeters et al., 1992).
The present acquisition results differ from the results reported by Savage et al. (1999). In their rat study using DMTP,
they did not find differences in the number of trials that the subjects required to meet the acquisition criterion, even though
they used the same criterion as we did (90% correct responses during three consecutive sessions).
The absence of a DOE acquisition effect in Savage et al.’s (1999) work versus our finding of a DOE effect may be explained
by a task complexity (difficulty) hypothesis. This hypothesis was described by Estévez, Fuentes, Marí-Beffa, González, and
Álvarez (2001) who reported that increasing the difficulty of a discrimination task for children allowed them to observe
the contribution of DOP training in the speed of acquisition. Comparing the focal two rat studies, Savages et al.’s DO and
NDO rats all mastered their task in about 12 sessions, while in our study the rat groups took on average between 18 and 50
sessions depending on age and DO versus NDO. From these findings, we may conclude that our task with a non-spatial cue
was more difficult than that in the Savage et al. experiment using a spatial cue.
Our findings parallel those of Estévez et al. (2001), who concluded from their data that the difficulty of the task is a relevant
factor to consider using differential outcomes procedures because difficulty can determine detection of the presence (or
absence) of a DOE acquisition effect. In other words, if the task is too easy to learn, we will not observe the contribution of
DOP. Our results contrasted with Savage et al.’s acquisition data are consistent with Estévez et al.’s (2001) hypothesis. The
two-choice discrimination task used in the present study allowed us to observe differences in the speed of acquisition; we
argue that these results are attributable to the greater difficulty of our task than the more easily learned matching-to-position
task of Savage et al. (1999).
The results of the present study are similar to the results reported by Flores and Mateos (2010) using a two-choice
discrimination task. They observed faster acquisition in rats trained with a DO versus NDO procedure wherein different
probabilities of reinforcement were used as the two different outcomes. Other work also has reported a DOE using different
probabilities of reinforcement as differential outcomes (e.g., DeLong & Wasserman, 1981).
Our results observed during the delay phase are consistent with those previously reported in the literature and replicate
those reported by Savage et al. (1999), who observed less decrease in the percentage of correct responses under delayed
conditions in groups trained with differential outcomes. Specifically, we found a clear difference in the performance of A-
DO and A-NDO rats, observing less decrease in the percentage of correct responses for rats in A-DO groups as delay was
lengthened than in the A-NDO. A smaller but similar positive DOE effect on performance was found in the young rats as well.
Thus, for both groups, the DOP enabled the rats to better bridge the temporal gap between the cue and the correct choice;
the beneficial effects of DOP were greater for aged animals than young animals.
As a whole, the present findings can be integrated with the evidence that suggests that using differential outcomes
procedures contributes to both learning and memory performance in subjects which are challenged. We believe this suggests
that the DOP may be a useful training procedure for those with developmental disabilities and/or memory impairments
induced by time, drugs, or brain damage. Indeed, some recent studies have reported and discussed the DOP as a pedagogical
tool which enhances learning of different topics (Miller, Waugh, & Chambers, 2002; Mok et al., 2010), and improves face
recognition in patients with alcohol dementia (Hochhalter et al., 2000), in children and adults with Down syndrome (Esteban,
Plaza, López-Crespo, Vivas, & Estévez, 2014; Estévez, Fuentes, Overmier, & González, 2003), and in older adults with age
related memory deficits (López-Crespo, Plaza, Fuentes, & Estévez, 2009).
Finally, the results reported in this study allow us to confirm the contribution made by DOP both to learning and to memory
based performance in aged subjects. Although the results do not enable us to disambiguate the possible mechanisms by
which DOP facilitates learning and memory-based performance, they do foster future efforts for the development of applied
behavioral strategies and their usage in the therapeutic treatment of age related disorders and possibly other memory
disorders.

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