Selective attention is a primary determinant of the relationship between working memory and general learning ability in outbred mice

Kolata, Stefan; Light, Kenneth; Grossman, Henya C.; Hale, Gregory; Matzel, Louis D.

doi:10.1101/lm.408507

Cited by 60 publications

(83 citation statements)

References 23 publications

(30 reference statements)

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“…In previous studies, secondary factors were occasionally observed, but were often difficult to interpret, suggesting that they were not extracting anything meaningful about the nature of the animals' cognition and were instead most likely due to chance. This is consistent with the relatively small amount of variance (typically less then 15%) accounted for by these factors (Matzel et al, 2003;Matzel et al, 2005;Kolata et al, 2005;Kolata et al, 2007).A subset of the animals reported here was also tested on two additional tasks (spatial win-stay and reinforced alternation) as well as the five tasks in the primary learning battery. It was hypothesized that these two tasks plus the spatial water maze would share a single domainspecific factor because of their common dependence on the hippocampus (O' Keefe & Speakman, 1987;Woods et al, 2000;Moser et al, 1995).…”

supporting

confidence: 81%

“…Similarly, we reported finding a substantial positive correlation between the aggregate performance of mice in a battery of learning tasks and their ability to withstand competing demands on working memory (Kolata et al, 2005). Furthermore, we found that one aspect of working memory, selective attention, was most strongly predictive of general learning abilities (Kolata et al, 2007). Taken together, our previous work suggests a hierarchical structure of cognitive abilities in mice with domain general abilities, such as working memory, influencing domain specific abilities, such as spatial ability.…”

supporting

confidence: 67%

“…It therefore appears from these results that while any individual learning task draws on specific domains of abilities (e.g. spatial) there also exists some learning-specific common factor that influences performance on all tasks.Our previous studies have suggested that the mechanisms underlying general learning abilities in mice are similar to those implicated in general intelligence in humans (Kolata et al, 2005(Kolata et al, , 2007. For instance, human studies have indicated that working memory capacity covaries with general intelligence (Colom, Rbello, Palacios, Juan-Espinosa, & Kyllonen, 2004;Conway, Kane, & Engle, 2003;Conway, Cowan, Bunting, Therriault, & Scott, 2002;Engle, Tuholski, Laughlin, & Conway, 1999).…”

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confidence: 93%

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Domain-specific and domain-general learning factors are expressed in genetically heterogeneous CD-1 mice

2008

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It has been established that both domain-specific (e.g. spatial) as well as domain-general (general intelligence) factors influence human cognition. However, the separation of these processes has rarely been attempted in studies using laboratory animals. Previously, we have found that the performances of outbred mice across a wide range of learning tasks correlate in such a way that a single factor can explain 30-44% of the variance between animals. This general learning factor is in some ways qualitatively and quantitatively analogous to general intelligence in humans. The complete structure of cognition in mice, however, has not been explored due to the limited sample sizes of our previous analyses. Here we report a combined analysis from 241 CD-1 mice tested in five primary learning tasks, and a subset of mice tested in two additional learning tasks. At least two (possibly three) of the seven learning tasks placed explicit demands on spatial and/or hippocampusdependent processing abilities. Consistent with previous findings, we report a robust general factor influencing learning in mice that accounted for 38% of the variance across tasks. In addition, a domain-specific factor was found to account for performance on that subset of tasks that shared a dependence on hippocampal and/or spatial processing. These results provide further evidence for a general learning/cognitive factor in genetically heterogeneous mice. Furthermore (and similar to human cognitive performance), these results suggest a hierarchical structure to cognitive processes in this genetically heterogeneous species. KeywordsIntelligence; Working Memory; Learning; Cognitive Abilities; Hippocampus; Spatial Learning; Mice For much of the history of animal studies of learning and memory, research has focused primarily on the processes and mechanisms that regulate single domains of learning (e.g., spatial abilities or Pavlovian conditioning). While this tactic has been successful in delineating the neuroanatomical substrates of certain forms of learning (e.g., Christian & Thompson;2003;Eichenbaum, 2000;Phelps & LeDoux, 2005;White & McDonald, 2002) it has left unexplored those aspects of learning that are common across all domains. Conversely, studies of humans have focused extensively on the mechanisms that underlie general influences that impinge on all cognitive abilities (i.e., general intelligence). However, such studies are constrained by certain practical and ethical considerations that do not similarly limit studies of Corresponding Author: Louis D. Matzel, Department of Psychology, Rutgers University, Piscataway, NJ 08854, Email: Matzel@rci.rutgers.edu, Phone: 732/445-5940, Fax: 732/445-2263. Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final citable form. Please note tha...

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confidence: 81%

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confidence: 67%

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confidence: 93%

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Domain-specific and domain-general learning factors are expressed in genetically heterogeneous CD-1 mice

2008

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“…To quantify individual differences in learning among mice, a variant of the procedures previously reported was used (Matzel et al 2003(Matzel et al , 2006Kolata et al 2005Kolata et al , 2007Kolata et al , 2008). All animals were tested in a series of six independent learning tasks (Lashley III Maze, passive avoidance, spatial water maze, odor discrimination, and fear conditioning) that place unique sensory, motor, motivational, and information processing demands on the animals.…”

Section: Behavioral Training and Testingmentioning

confidence: 99%

Age-related declines in general cognitive abilities of Balb/C mice are associated with disparities in working memory, body weight, and general activity

Matzel¹,

Grossman²,

Light³

et al. 2008

Learn. Mem.

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A defining characteristic of age-related cognitive decline is a deficit in general cognitive performance. Here we use a testing and analysis regimen that allows us to characterize the general learning abilities of young (3-5 mo old) and aged (19-21 mo old) male and female Balb/C mice. Animals' performance was assessed on a battery of seven diverse learning tasks. Aged animals exhibited deficits in five of the seven tasks and ranked significantly lower than their young counterparts in general learning abilities (aggregate performance across the battery of tasks). Aging added variability to common core performance (i.e., general learning ability), which translated into increased variability on the individual cognitive tasks. Relatedly, general learning abilities did not differ between the two ages among the best quartile of learners (i.e., cognitive abilities were spared in a subsample of the aged animals). Additionally, working memory capacity (resistance to interference) and duration (resistance to decay) accounted for significantly more of the variability in general learning abilities in aged relative to young animals. Tests of 15 noncognitive performance variables indicated that an increase in body weight (and an associtaed decrease in general activity) was characteristic of those aged animals which exhibited deficient general learning abilities. These results suggest the possibility that general cognitive deficits in aged animals reflect a failure of specific components of the working memory system, and may be related to variations in body weight and an associated decrease in activity.Broad and general learning deficits are a defining feature of the cognitive phenotype of elderly humans. However, investigations of the neurological basis of age-related cognitive decline (particularly in nonhuman animals) have typically focused on specific types or classes of cognitive abilities. Although the effects of aging on hippocampus-dependent cognitive processes have been well documented (for reviews, see Gallagher and Rapp 1997;Rosenzweig and Barnes 2003), and multivariate approaches to the assessment of the impact of aging on noncognitive classes of behavior have been reported (e.g., Markowska and Breckler 1999), systematic efforts to describe learning impairments that transcend single domains of cognitive abilities have been rare. Notwithstanding the success of efforts to characterize the impact of aging on cognitive "domains," the lack of attention to domain-independent (i.e., "general") cognitive abilities limits the functional application of these conclusions. The absence of animal studies of age-related declines in general cognitive abilities is especially problematic in light of data obtained from human test batteries which indicate that age-related learning deficits transcend specific domains of learning and are expressed independently of the sensory, motor, motivational, or information processing demands of individual learning tasks. It has been estimated that as much as 25%-50% of the age-related decline in c...

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“…A subsequent study of correlations between WM abilities and g in mice attempted to determine the components of WM still further (43). It involved tests of WM retention time, WM retention capacity, as well as capacities for selective attention.…”

Section: Inability Tomentioning

confidence: 99%

Evolution of working memory

Carruthers

2013

Proc. Natl. Acad. Sci. U.S.A.

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Working memory (WM) is fundamental to many aspects of human life, including learning, speech and text comprehension, prospection and future planning, and explicit "system 2" forms of reasoning, as well as overlapping heavily with fluid general intelligence. WM has been intensively studied for many decades, and there is a growing consensus about its nature, its components, and its signature limits. Remarkably, given its central importance in human life, there has been very little comparative investigation of WM abilities across species. Consequently, much remains unknown about the evolution of this important human capacity. Some questions can be tentatively answered from the existing comparative literature. Even studies that were not intended to do so can nonetheless shed light on the WM capacities of nonhuman animals. However, many questions remain.T he nature of human working memory (WM) has been extensively investigated, with thousands of articles and books on the topic produced over the last half-century. Some of the main findings of this research will be outlined shortly. However, we know hardly anything about how WM evolved. For that (if we are to go beyond plausible speculation), we need detailed comparative studies. However, remarkably few such studies have been conducted, as we will see. Nevertheless, the emerging consensus about the nature of human WM allows us to frame a series of questions or alternative hypotheses concerning the possible differences between human and animal WM. Some of these can be answered, at least tentatively, from the results of existing work. However, they should also be used to frame and guide future comparative experiments. Working Memory in HumansWM is the domain-general subsystem of the mind that enables one to activate and sustain (sometimes via active rehearsal) a set of mental representations for further manipulation and processing. The contents of working memory are generally thought to be conscious. Indeed, many identify the two constructs, maintaining that representations become conscious by gaining entry into WM (1). WM is generally thought to consist of an executive component that is distributed in areas of the frontal lobes working together with sensory cortical regions in any of the various sense modalities, which interact through attentional processes (2). It is also widely accepted that WM is quite limited in span, restricted to three or four chunks of information at any one time (3). Moreover, there are significant and stable individual differences in WM abilities between people, and these have been found to predict comparative performance in many other cognitive domains (4). Indeed, they account for most (if not all) of the variance in fluid general intelligence, or g (5).The primary mechanism of WM is thought to be executively controlled attention (2, 6). It is by targeting attention at representations in sensory areas that the latter gain entry into WM, and in the same manner they can be maintained there through sustained attention. Attention itself is though...

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Selective attention is a primary determinant of the relationship between working memory and general learning ability in outbred mice

Cited by 60 publications

References 23 publications

Domain-specific and domain-general learning factors are expressed in genetically heterogeneous CD-1 mice

Domain-specific and domain-general learning factors are expressed in genetically heterogeneous CD-1 mice

Age-related declines in general cognitive abilities of Balb/C mice are associated with disparities in working memory, body weight, and general activity

Evolution of working memory

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