Working Memory Training Pr

Current Biology 20, 777–782, April 27, 2010 ª2010 Elsevier Ltd All rights reserved DOI 10.1016/j.cub.2010.02.034

Reportomotes

General Cognitive Abilitiesin Genetically Heterogeneous Mice

Kenneth R. Light,1 Stefan Kolata,1 Christopher Wass,1

Alexander Denman-Brice,1 Ryan Zagalsky,1

and Louis D. Matzel1,*1Program in Behavioral Neuroscience, Department ofPsychology, Rutgers University, Piscataway, NJ 08854, USA

Summary

In both humans and mice, the efficacy of working memorycapacity and its related process, selective attention, are

each strongly predictive of individuals’ aggregate perfor-mance in cognitive test batteries [1–9]. Because working

memory is taxed during most cognitive tasks, the efficacyof working memory may have a causal influence on individ-

uals’ performance on tests of ‘‘intelligence’’ [10, 11]. Despitethe attention this has received, supporting evidence has

been largely correlational in nature (but see [12]). Here,genetically heterogeneous mice were assessed on a bat-

tery of five learning tasks. Animals’ aggregate performanceacross the tasks was used to estimate their general cognitive

abilities, a trait that is in some respects analogous to intelli-gence [13, 14]. Working memory training promoted an

increase in animals’ selective attention and their aggregateperformance on these tasks. This enhancement of general

cognitive performance by working memory training wasattenuated if its selective attention demands were reduced.

These results provide evidence that the efficacy of working

memory capacity and selective attention may be causallyrelated to an animal’s general cognitive performance and

provide a framework for behavioral strategies to promotethose abilities. Furthermore, the pattern of behavior reported

here reflects a conservation of the processes that regulategeneral cognitive performance in humans and infrahuman

animals.

Results

Working Memory Exercise Promotes Selective Attentionand General Cognitive Performance

Procedures and results from individual tests are presented inthe Supplemental Information available online. One group ofanimals received 12 days of training wherein they performedconcurrently in two eight-choice radial arm mazes. This taskwas designed to promote a heavy reliance on all aspects ofworking memory (including aspects of short-term mainte-nance, capacity, and selective attention) and has beendescribed previously [8, 9]. A second group received compa-rable handling absent any working memory training. Whenboth groups of mice were subsequently tested on a mouseanalog [9] of the human Stroop test, mice that received thisworking memory training performed significantly better thananimals that had not undergone training. That is, task-relevantinterference provoked fewer errors in animals that hadpreviously undergone working memory training [Figure 1B;

*Correspondence: matzel@rci.rutgers.edu

F(1,25) = 8.20, p < 0.01], suggesting that this training promotedan increase in the efficacy of selective attention.

All animals were then tested on five independent learningtasks (passive avoidance, odor discrimination, associativefear conditioning, egocentric navigation in a Lashley maze,and spatial navigation in a water maze). Results from individualtasks in the learning battery are presented in the SupplementalInformation. To obtain general learning scores for all mice, wesubjected acquisition data from the five learning tasks toa principal components analysis. A primary factor wasextracted with an eigenvalue of 1.51, which accounted for30% of the variance across animals. From this primary factor,factor scores were extracted to represent each animal’sgeneral learning ability. Factor scores, which are analogousto an average z score of an animal’s performance across alltasks, provide a sensitive index of an individual’s aggregateperformance in the learning battery. However, the number ofsubjects used here is somewhat small by factor analytic stan-dards. Therefore, to verify the accuracy of these factor scoresas descriptors of general learning performance, the factorscores were compared to each animal’s average rank perfor-mance (relative to others in the sample) across all five learningtasks (a method that has been previously reported [13]). Factorscores and average ranks were significantly correlated [r(25) =0.61, p < 0.001]. Because factor scores are presumed to bea more precise measure of an animal’s aggregate performanceacross all tasks, these scores were used in all subsequentanalyses to compare the performance of groups of animals.

Mice trained on the concurrent radial arm maze task hadsignificantly higher general learning scores than did animalsthat were not subjected to this working memory training [Fig-ure 1C; F(1,25) = 4.48, p < 0.05; Cohen’s d effect size = 0.94].It was possible that working memory training differentiallyimproved general learning scores in a subset of mice (e.g.,mice from different regions of the distribution of generallearning abilities). To assess this, we compared factor scoresfor the top and bottom performers on the learning batteryacross animals that had received or had not received workingmemory training (Figure 1D). The top half of mice that hadundergone working memory training had significantly highergeneral learning abilities than the top half of animals that hadnot received working memory training [F(1,11) = 6.88, p <0.05]. A similar difference was observed in those animalsfrom the bottom halves of the distribution of learning abilities[F(1,11) = 13.92, p < 0.005], suggesting that working memorytraining promotes an improvement in general learning perfor-mance regardless of an animal’s position in the distributionof learning abilities.

In this experiment, animals that underwent working memorytraining exhibited a commensurate increase in their aggregateperformance in a battery of diverse learning tasks. Two alter-native explanations for these results are possible. First, it isconceivable that any manipulation outside of the home cagewould have resulted in an increase in general learning abilitiessimply because it rescues the animals from the environmentaldeprivation of the home cage. However, this result stands incontrast to previous attempts to manipulate general learningabilities of mice through extensive and repeated exposure to

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Figure 1. Working Memory Training Promotes

Improvements in General Cognitive Performance

(A) Animals were first trained to asymptote in two

radial arm mazes and then performed in the two

mazes concurrently, i.e., alternating choices in

the two mazes within single test trials (working

memory training). A second group received no

training during this phase. Plotted is the total

number of errors committed on each trial (across

the two mazes) during twelve such trials.

(B) Animals performed an odor discrimination

task and a visual discrimination task in each of

two distinct contexts. At the time of six test trials,

the odor and visual cues were simultaneously

presented in the context that signaled the

odor discrimination or the visual discrimination.

This constituted a mouse analog of the human

Stroop test, where task-relevant distracters

must be ignored in order for the subject to

perform efficiently. The average number of errors

across the six test trials is plotted as a function of

group (i.e., either working memory trained [WM]

or not). These results indicate that working

memory training facilitates selective attention

performance.

(C) From principal components analysis of all

learning tasks, each animal was assigned a factor

score to represent its general learning ability.

Average factor scores for each group are plotted.

Prior working memory training promoted an

improvement in general learning performance.

(D) From principal components analysis of all learning tasks, general learning ability (primary factor score) is plotted as a function of group for both the top

and bottom halves of the distribution of general learning abilities. Working memory training supported improved general learning abilities in animals drawn

from both halves of the distribution.

Error bars indicate standard error of the mean.

Current Biology Vol 20 No 8778

novel environments, a treatment that had no effect on generallearning performance [15]. Relatedly, we have observed thatworking memory training promotes an increase in exploration(data not shown), raising the possibility that learning is facili-tated as a consequence of the increase in exploration (andthus contact with environmental contingencies that supportlearning). However, we have tested this possibility by directlyincreasing exploratory tendencies by adapting mice to a seriesof novel environments. The widespread increase in explor-atory behaviors promoted by this adaptation to novel environ-ments supported no increase in general learning abilities(measured identically to that reported here [15]). Therefore,we can conclude that simply increasing exploration is insuffi-cient to increase general learning abilities. (It is worth notingthat in work presently under review, we have found that therelationship between exploration and general learning abilitiesis actually a consequence of variations in learning abilities,wherein learning impacts the rate of habituation to a novelenvironment.) In total, these results indicate that workingmemory training promotes an improvement in general cogni-tive abilities, and that it does so independently of any effectof that training on exploratory tendencies or other nonspecificconsequences of exposure to environments outside of thehome cage.

The Effectiveness of Working Memory Exercise

Is Dependent on Its Taxation of Selective AttentionA second experiment was designed to determine the compo-nent of working memory that is most relevant to the impact ofworking memory training on general cognitive performance.Previous research in our laboratory has indicated that per-formance indicative of selective attention is more highly

correlated with general learning abilities than are measuresof simple memory span or duration [9]. Consequently, reduc-ing the selective attention component of working memorytraining should reduce the effect of that training on generallearning abilities. In the working memory training describedabove, animals were required to maintain a memory of twosets of choices that were guided by a common, overlappingset of visual cues, thus taxing both the animals’ ability to main-tain information while simultaneously segregating that infor-mation according to the task (maze) that it was specific to.In humans, cue overlap (and the selective attention that itdemands) has been shown by Conway and Engle [16] to behighly relevant to the relationship between working memoryand performance on tests indicative of general fluid intelli-gence. In combination with the results of Kolata et al. [9], thesedata suggest that in the previous experiment, the presumeddemands on selective attention imposed by the overlappingcues are a particularly strong candidate for the componentof working memory training responsible for the observedincrease in general learning abilities.

In the second experiment, two groups received 12 daysof working memory training (Figure 2A), and a third groupreceived comparable handling and deprivation conditions.Of the two groups that received working memory training,one was treated identically to the comparable group in the pre-vious experiment, i.e., trained on two mazes in a single roomsuch that the mazes shared overlapping cues. The secondgroup was trained on the same two mazes, but the mazeswere physically separated by an opaque (floor to ceiling)curtain with distinct cues on each side. When so arranged,the two mazes shared no cues in common. When the threegroups of mice were subsequently tested in the mouse analog

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Figure 2. Selective Attention Underlies the

Effects of Working Memory Training

(A) Animals were first trained to asymptote in two

radial arm mazes and then performed in the two

mazes concurrently, i.e., alternating choices in

the two mazes within single test trials (working

memory training). One group of animals received

training wherein the two mazes shared overlap-

ping visual cues (which guide the animals’

search), and one group received training on

mazes that were explicitly separated, sharing no

overlapping visual cues. The total number of

errors committed on each trial (across the two

mazes) during twelve such trials is plotted.

A third group received only equivalent handling

but did not perform in the mazes.

(B) Animals performed an odor discrimination

task and a visual discrimination task in each of

two distinct contexts. At the time of six test trials,

the odor and visual cues were simultaneously

presented in the context that signaled the

odor discrimination or the visual discrimination.

This constituted a mouse analog of the human

Stroop test, where task-relevant distracters

must be ignored in order for the animal to perform

efficiently. The total errors across the six test

trials are plotted as a function of group (i.e.,

working memory training with overlapping or no

overlapping visual cues, or no working memory

training). Prior working memory training facilitated selective attention, and that effect was accentuated if that training required animals to segregate infor-

mation related to shared (overlapping) cues.

(C) From principal components analysis of all learning tasks, general learning ability (primary factor score) is plotted as a function of group. Prior working

memory training promoted an improvement in general learning performance, and that effect was accentuated if that training required animals to segregate

information related to shared (overlapping) cues.

(D) From principal components analysis of all learning tasks, general learning ability (primary factor score) is plotted as a function of group for both the top

and bottom halves of the distribution of general learning abilities. Working memory training supported improved general learning abilities in animals drawn

from both halves of the distribution, and that effect was accentuated if that training required animals to segregate information related to shared (overlapping)

cues.

Error bars indicate standard error of the mean.

Working Memory Training and Intelligence779

of the human Stroop test, there was a strong trend towarda main effect of training history [Figure 2B; F(2,24) = 3.31, p =0.054]. Planned comparisons revealed a significant differencein the performance on the Stroop test between mice thatreceived working memory training with overlapping cues andeach of the remaining two groups (p < 0.05) but no differencebetween the animals trained with no overlapping cues andanimals not subject to any working memory training. Theseresults indicate that the added selective attention loadrequired to perform the working memory task when cues over-lapped promoted superior performance on the subsequenttest of selective attention. It is noted that the two forms ofradial arm maze training (with overlapping or nonoverlappingcues) made very different demands on the animals, and it ispossible that the difficulty performing these tasks (ratherthan selective attention demands per se) may promote differ-ences in performance in tests of selective attention. Toaddress whether the two radial arm maze tasks varied in diffi-culty, we performed a factorial analysis of variance on theacquisition data in the black maze for groups trained with over-lapping or nonoverlapping visual cues, and no differencebetween groups was observed [F(1,19) = 0.79]. Moreover, at test was performed to compare the performance of the twogroups on the last trial of this training, and again, no differencewas observed [t(19) = 1.43]. These results suggest that the twotasks were similarly difficult and thus that task difficulty wasnot a principal determinant of the observed improvement inselective attention.

Results from individual tasks in the learning battery are pre-sented in the Supplemental Information. In this experiment,a principal components analysis of learning performanceextracted a single factor with an eigenvalue of 1.73, whichaccounted for 35% of the variance in performance of individualanimals across all tasks. From this analysis, factor scores wereextracted that represented the general learning performance ofindividual animals. As in the previous experiment, we verifiedthe accuracy of these factor scores as descriptors of animals’aggregate performance in the learning battery by assessingthe correlation of these scores with animals’ average rankperformance across all five learning tasks. The two measureswere significantly correlated [r(25) = 0.84, p < 0.0001].

When factor scores from the three treatment conditionswere compared, a main effect of treatment was observed [Fig-ure 2C; F(2,24) = 10.57, p < 0.001, u2 effect size = 0.54]. Posthoc comparisons of factor scores revealed significant differ-ences between the group that received overlapping cuesduring working memory training and the group that receivedno overlapping cues during this training (p < 0.05) and animalsthat received no working memory training (p < 0.001). Lastly,a difference was observed between the group that receivedworking memory training with no overlapping cues and thegroup that received no working memory training (p < 0.05).

Again we assessed whether working memory training differ-entially affected the general learning performance of animalsdrawn from the top or bottom half of the distribution of learningabilities (Figure 2D). In the top half of the distribution, there was

Current Biology Vol 20 No 8780

a main effect of group [F(2,10) = 8.47, p < 0.01]. Plannedcomparisons revealed a significant difference between thegroup that received working memory training with overlappingcues and control animals that received no working memorytraining (p < 0.005). However, trends were seen toward differ-ences between mice that received working memory trainingwith overlapping cues relative to those that received thistraining with no overlapping cues (p = 0.09), as well as betweenmice that received working memory training with no overlap-ping cues and animals that had received no working memorytraining (p = 0.06). In the bottom half of the distribution oflearning abilities, the same pattern of results was observed.There was a significant main effect of group [F(2,10) = 13.97,p < 0.005]. Planned comparisons revealed significant differ-ences in general learning performance between mice thatreceived working memory training with overlapping cues andanimals that received no working memory training (p <0.001), mice that received working memory training with nooverlapping cues and those that did not receive workingmemory training (p < 0.05), and mice that received workingmemory training with overlapping or no overlapping cues(p < 0.05). Thus, working memory training again promoted animprovement in general learning abilities in animals in boththe top and bottom halves of the distribution of abilities.Importantly, working memory training without overlappingcues produced performances intermediate to training withoverlapping cues and no training in both the top and bottomhalves of the distribution.

This experiment provides a second demonstration thatworking memory training facilitates the implementation ofselective attention and promotes a commensurate increasein general learning abilities. When the selective attention loadof the complex radial arm maze task was reduced, the effectof working memory training on general learning abilities wassimilarly attenuated (although not eliminated). This diminishedyet persistent influence of working memory training with a lowselective attention load on general learning abilities can beaccounted for in two ways. First, it is possible that workingmemory training by itself, regardless of selective attentionload, is sufficient to promote an increase in general learningabilities. Consistent with this possibility, variations in workingmemory span have been determined to predict generallearning abilities in mice as well as general intelligence inhumans [10, 17], although they do so to a lesser degree thantests of working memory that more heavily tax the selectiveattention system. Another possibility is that overlapping cueswere simply reduced rather than eliminated, i.e., the animalsmay have used uncontrolled (i.e., undetected) aspects of thetraining context to guide their behavior. From the presentdata, we cannot determine which of these two, if either,accounts for the residual impact of working memory trainingwith a low selective attention load on the aggregate generallearning abilities of mice.

Discussion

The present set of experiments provides evidence that trainingregimens that ‘‘exercise’’ working memory promote anincrease in the efficacy of selective attention and a commensu-rate increase in general learning abilities. We have extendedprevious results obtained with human subjects [12, 18–22] bycomparing a working memory training regimen that specifi-cally taxes the selective attention system to one with a nomi-nally reduced selective attention load and find that the

selective attention load of this training is a critical determinantof the consequent improvement in general cognitive perfor-mance. This provides evidence that training regimens thatheavily tax the selective attention system have a particularlypotent capacity to increase general learning abilities in mice.

In humans, a diverse set of training methods have beenestablished that promote aspects of attention and self-regula-tion [22]. In combination with the parameters established herethat promote selective attention and general learning abilities,the capacity to modulate attention in humans has importantimplications for understanding intelligence and the modulationof this trait in humans. For instance, training programs thatpromote attention have been determined to have modesteffects on children’s performance on tests considered to beindicative of fluid intelligence [20, 21, 23], and this effect isaccentuated in children that express attention deficit disor-ders [18]. Qualitatively similar results have been observed inaged humans [24]. In combination, these results have begunto converge on the conclusion that the capacity for attentioncan be modified through structured training and that thistraining may commensurately impact performance thatreflects variations in intelligence.

One might ask whether the beneficial effects of workingmemory training reflect a consequence of that training orsimply reflect the experientially deprived state of the controlmice that did not receive training outside of the home cage—i.e., would any experience outside of the home cage havesimilar beneficial effects on general learning abilities? Relat-edly, it is possible that the manipulation of any correlate ofgeneral learning ability of mice might similarly impact thoseabilities. To assess these considerations, we have previouslydemonstrated that repeatedly exposing mice to novel environ-ments (for an amount of time comparable to that used here forthe implementation of working memory training) promotes anincrease in the animals’ subsequent exploration of new envi-ronments. However, this exposure to novel environmentsand the resultant increase in exploratory behaviors had noimpact on the animals’ general learning performance [15],despite the fact that native exploratory propensity has beenrepeatedly determined to strongly predict general learningabilities [13, 25, 26].

It is worth noting that in a manuscript currently under review,we report that the expression of a cluster of genes related todopamine signaling in the prefrontal cortex is directly relatedto the aggregate performance of mice in the cognitive testbattery described here, and the dopaminergic processes reg-ulated by these genes have been demonstrated to contributeto the efficacy of working memory [27–29]. It is thus temptingto speculate that working memory training, like that imposedhere, might upregulate the expression of these same genes,providing a potential epigenetic mechanism for the impact ofworking memory training on general cognitive abilities.

It has long been recognized that the processing compo-nents of the working memory system such as working memorycapacity and/or selective attention are strongly correlated withhumans’ performance on tests indicative of intelligence [30].‘‘Higher cognitive functions’’ (such as reasoning, comprehen-sion, and learning) are the hallmark of contemporary intelli-gence test batteries and form common colloquial descriptionsof ‘‘intelligence.’’ Thus, it is not surprising that workingmemory (or at least some of its subcomponents) have cometo be viewed by some as the potential latent factor thatunderlies general (fluid) cognitive abilities, i.e., intelligence[17, 31]. Accordingly, variations in working memory efficacy

Working Memory Training and Intelligence781

have been proposed to regulate individual differences inintelligence. Although theoretically compelling, evidence forthis causal relationship has been difficult to attain [10, 11].The results presented here, wherein we have demonstratedthat working memory training has a direct commensurateinfluence on general learning abilities, provide tentative sup-port for a causal relationship between the process (workingmemory) and the trait (general cognitive ability).

Experimental Procedures

Experiment 1 Subjects

Twenty-nine outbred CD-1 mice were obtained at 55 days of age, an age

typical of previous experiments in our laboratory, and were housed individ-

ually and maintained on ad libitum food and water unless noted otherwise in

a temperature-controlled vivarium on a 12 hr light/dark cycle. The mice were

acclimated to the vivarium for 1 week and were subsequently handled

(removed from the home cage and held by the experimenter for 60 s/day)

for 1 week prior to the start of training. Owing to a scheduling error, three

animals could not complete the experiment, resulting in final group

sizes of 13.

Experiment 1 Design

This experiment was a two-group, between-subjects design. Native explor-

atory tendencies are a good predictor of general learning abilities [13, 26],

and so animals were assigned to one of two groups based on their perfor-

mance on a pretest for propensity for exploration in an elevated plus

maze (see Supplemental Information). Working memory training was admin-

istered to one group, while the other was equivalently handled. Training and

testing were identical to that used previously in our laboratory [15, 25] and

are described in detail in the Supplemental Information. In brief, mice

were trained to asymptote on two distinct radial arm mazes, where the

animals collected food at the end of each of eight arms. The mazes were

located in the same room such that they shared common extramaze

visual cues (patterns of lights, pictures, and architectural details that are

used by the animal to guide its search). After performance in each of the

two mazes stabilized, animals then were tested on each of the two mazes

each day (3 hr intertrial interval) for 3 days (the order of testing in the two

mazes alternated across days). Subsequent to this initial training, the

animals then performed concurrently on both mazes once a day for 12 days

(constituting working memory training). During this training, mice alternated

choices in the two mazes and consequently were required to maintain

a memory of the choices in each maze and to segregate those memories

despite the overlapping extramaze visual cues. Thus, this training taxed

both the maintenance of information as well as working memory capacity

and selective attention.

Four days after working memory training (at 112 days of age), mice began

testing on a battery of five learning tasks (Lashley maze, passive avoidance,

spatial water maze, odor discrimination, and associative fear conditioning),

which has been described previously [13, 15, 26]. One week after comple-

tion of the learning battery, mice were tested for selective attention abilities

in a mouse-adapted version of the Stroop test [14]. In brief, mice were

trained to find food by choosing a correct odor (from three possible) in

one context and a correct visual stimulus (from three possible) in a second

context. In the critical test, mice were tested separately in the odor and

visual contexts; during the test trial, both sets of cues were presented simul-

taneously. To perform efficiently during this test trial, mice must ignore

those cues that are relevant to the context other than the current test

context and, in doing so, discriminate between cues relevant only to perfor-

mance in the current test context (e.g., visual cues should be ignored when

tested in the odor discrimination context). As we describe in detail else-

where [9], although no test is process pure, this test makes no nominal

demands on working memory span or duration but instead requires animals

to focus on task-specific cues while ignoring task-relevant distracters and is

thus conceptually consistent with contemporary descriptions of selective

attention [32, 33].

Experiment 2 Subjects

Thirty mice arrived in our laboratory at 45 days of age and were maintained

and tested as in experiment 1. Owing to a training error, three animals could

not complete the experiment, resulting in final group sizes of nine (working

memory training with overlapping cues), nine (working memory training with

no overlapping cues), and nine (no working memory training).

Experiment 2 Design

As in experiment 1, mice were all assessed in the elevated plus maze at

approximately 80 days of age. They were then assigned to one of three

groups, balanced for exploration in the elevated plus maze. One group

received radial arm maze training as described in experiment 1. A second

group received radial arm maze training as described in experiment 1,

although a floor-to-ceiling opaque curtain with a different set of visual

cues on each side was placed between the two radial arm mazes. This

curtain effectively split the room in half, leaving each maze in what was

essentially a distinct room with distinct extramaze cues. The relevant effect

of this alteration on the training of the second group was to have mice

trained on the same two radial arm mazes used for training the first group,

although in this case, the mazes shared no common cues. Because the

animals trained under these latter conditions need not segregate common

information according to the relevant maze, this training imposed reduced

demands on selective attention. A third group received no working memory

exercise. Mice in this group received equivalent food deprivation and food

reward (delivered in their home cages), as well as handling equivalent to

that administered to the working memory training groups.

Supplemental Information

Supplemental Information includes Supplemental Results and Supple-

mental Experimental Procedures and can be found with this article online

at doi:10.1016/j.cub.2010.02.034.

Acknowledgments

This work was supported by the National Institute on Aging (AG022698) and

the Busch Foundation (to L.D.M.).

Received: November 2, 2009

Revised: February 8, 2010

Accepted: February 9, 2010

Published online: March 25, 2010

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