Elsevier

Brain Research

Volume 1244, 9 December 2008, Pages 121-131
Brain Research

Research Report
Dedifferentiation in the visual cortex: An fMRI investigation of individual differences in older adults

https://doi.org/10.1016/j.brainres.2008.09.051Get rights and content

Abstract

Dedifferentiation, or decreased processing specificity, has been suggested to represent a ubiquitous characteristic of cognitive aging. In this study, we examined both age-related differences and intra-group differences in neural specificity in the ventral visual cortex for color, words, faces and places. Our results demonstrated that neural dedifferentiation was not ubiquitous across stimulus categories. Neural dedifferentiation was also relatively stable, across age, in a group of older adults. Older adults with more overall gray matter showed less neural dedifferentiation in the visual cortex. However, regional gray matter volume was not associated with neural dedifferentiation. We illustrate these effects using a discriminability metric, a signal detection theory measure, for neural dedifferentiation that takes into account both magnitude and variance of brain activation. The dedifferentiation measure provides a quantitative means to examine activation patterns and individual difference factors associated with neural dedifferentiation, and to test theories of behavioral dedifferentiation in cognitive aging literature.

Introduction

The dedifferentiation hypothesis posits that increasing age is associated with decreased processing specificity, manifested behaviorally by increased covariance in measures of distinct cognitive abilities. For example, it has been shown that with age comes an increase in the correlation among measures of different cognitive constructs such as memory, reasoning, perceptual speed, verbal knowledge, and fluency (Baltes and Lindenberger, 1997, Li et al., 2004), presumably through a decline in fundamental structural or functional neural resources, or both, across the adult lifespan (Lindenberger et al., 2001, Park et al., 2001, Park et al., 2004, Li et al., 2006). Developmentally, the emergence of neural processing specificity indicates neural differentiation. Therefore, the decreased neural processing specificity that occurs with age is denoted as age-related neural dedifferentiation.

An emergence of brain imaging methods, such as magnetic resonance imaging (MRI) have made it possible to examine behaviorally developed and supported hypotheses of age-related cognitive decline such as dedifferentiation, within the context of structural and functional brain imaging. Structural MRI results demonstrate that while the human brain undergoes widespread gray and white matter tissue atrophy, there is increased regional atrophy in the frontal cortex, caudate nucleus, hippocampus, and cerebellum (Raz et al., 2005). In terms of brain function, age-related neural dedifferentiation has been defined as a change in the spatial pattern of brain activation with age as a result of decreased neural specificity (Park et al., 2001, Park et al., 2004, Zarahn et al., 2007). Hereafter, the term differentiation is used to denote increased neural specificity, and the term dedifferentiation is used to denote decreased neural specificity. Patterns of brain activation that characterize neural dedifferentiation are more diffuse, in the contralateral brain region, or in a brain region that may or may not be related to task performance in younger adults. Evidence from functional MRI (fMRI) studies suggest that neural dedifferentiation may occur in regions of cortex involved in top-down control (prefrontal), associative binding (hippocampus and parahippocampus), neural object representations (ventral visual cortex), and in primary sensory cortices (Park et al., 2001, Park et al., 2003, Cabeza et al., 2004, Rajah and D'Esposito, 2005, Payer et al., 2006). Critically, previous research that has studied age-related changes in spatial activation patterns and their relation to cognitive performance and age has used qualitative measures of dedifferentiation (spatial overlap, or presence or absence of spatial activation differences). A quantitative measure of dedifferentiation that takes into account both magnitude and variance of activation would help examine not only age-related differences, but also could potentially be used as a tool to study individual differences within an aging cohort. In the present study, we thus used a quantitative approach to measure neural dedifferentiation in the ventral visual cortex.

The ventral visual cortex provides an excellent landscape to examine age-related differences in neural specificity. Numerous studies have provided evidence for the remarkable and robust capacity of the ventral visual cortex to develop specific regions for processing environmentally familiar stimuli such as faces, the human body, places, objects, words and letter strings, and colors under both passive viewing and task-related conditions (Epstein and Kanwisher, 1998, Kanwisher, 2000, Jobard et al., 2003, Downing et al., 2006). While older adults have demonstrated the capability to retain category specific activation in the ventral visual cortex (Madden et al., 2002, Brodtmann et al., 2003), older adults have also shown more generalized brain activity such that stimulus category-activated voxels overlap to a greater extent in old adults compared with young (Park et al., 2004, Payer et al., 2006). Thus, the study of neural dedifferentiation in the ventral visual cortex provides an opportunity to examine functional brain activation within brain regions shown to have reliable regional specificity in young adults (Epstein and Kanwisher, 1998, Kanwisher, 2000, Gegenfurtner, 2003, Jobard et al., 2003, Downing et al., 2006), and to examine the changes that occur with age (Park et al., 2004, Schmolesky et al., 2000, Godde et al., 2002). Further, as noticed above, a quantitative measure of neural dedifferentiation would facilitate the characterization of individual difference factors that are associated with dedifferentiation in the aging brain.

For example, while it is assumed that dedifferentiation continues to increase throughout the adult lifespan, previous literature has focused only on main effects of age. While indeed strong evidence has been shown to support that older adults are more dedifferentiated than young in the visual cortex (Park et al., 2004), it is also important to examine neural dedifferentiation as a function of age within an old adult sample. This presents an important application of a quantitative measure of neural specificity. It is also possible that normal age-related loss of gray matter volume within the ventral visual cortex, or throughout the brain, plays a role in dedifferentiated visual processing. That is, if neural dedifferentiation is accompanied by structural degeneration in the ventral visual cortex, a strong hypothesis would be that local neuronal integrity moderates the presence (or absence) of neural dedifferentiation. However, if global rather than, or in addition to, local brain volume is associated with dedifferentiation in the ventral visual cortex, this suggests that either other brain structures are important for neural specificity in the visual cortex, or that other functional brain networks are involved. While regional and global structural brain integrity are often cited as potential correlates of dedifferentiation (Park et al., 2001, Cabeza et al., 2004, Rajah and D'Esposito, 2005), neither has been directly examined, and we attempt to do this in the present study.

Overall, there were two primary goals for this study. The first goal was to apply a measure of discriminability, or neural selectivity, to quantitatively measure neural processing specificity (Afraz et al., 2006, Grill-Spector et al., 2007), see Fig. 2. The measure provided a means to examine whether old adults show dedifferentiation in the form of less neural specificity for stimuli localized in the ventral visual system. To assess whether old adults were activating more diffusely as a group compared with young adults, we compared the spatial variability of maximum response for young and old. The second primary goal of this study was to characterize the nature of neural dedifferentiation as an individual difference variable; we examined neural dedifferentiation as a function of age and regional and global brain volume. Specifically, the present study focused on measuring neural dedifferentiation in ventral visual cortex.

Section snippets

Color

The maximum Z statistic within localized color selective clusters for groups of young and old participants were within 6-mm of each other (within the spatial smoothing kernel of 6-mm FWHM). Therefore, a 1000-mm3 common group ROI (125 voxels) for young and old was centered on the average coordinates (MNI: − 30, − 82, − 19) of these peaks, from which young and old activation patterns were compared (see Fig. 1). We also found that subject-specific peaks were not more spatially distributed for old

Discussion

As predicted, our results are consistent with previous findings that young adults showed more neural specificity in the ventral visual cortex compared with old adults. Our results are novel in demonstrating that while dedifferentiation was shown to be ubiquitous in the sense that it occurred for all older adults regardless of age, dedifferentiation was not shown to be ubiquitous across stimulus categories. Young adults showed more neural specificity for faces and places compared with old

Participants

Participants were recruited from the local community of Urbana-Champaign, Illinois. Eligible participants had to (1) demonstrate strong right handedness, with a 75% or above on the Edinburgh Handedness Questionnaire (Oldfield, 1971), (2) be between the ages of 18 and 35 for young adults and between 55 and 80 years for older adults (3) score > 51 on the modified Mini-Mental Status Exam (mMMSE, (Stern et al., 1987)), a screening questionnaire to rule out potential neurological pathology, (4) score < 

Acknowledgments

We would like to thank Nancy Dodge, Holly Tracy, Edward Malkowski, Jennifer Kim, and Maritza Alvarado, and EPL laboratory for their help in data collection. We would also like to thank the National Institute on Aging (RO1 AG25667 and RO1 AG25032) and the Institute for the Study of Aging for their support of our research. Finally, we would like to thank reviewers for their helpful comments and suggestions on previous versions of the manuscript.

Disclosure statement

Appropriate approval and

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    Present address: School of Psychology, Adeilad Brigantia, Penrallt Road, Gwynedd LL57 2AS, U.K., Fax: +44 (0) 1248 38 2599.

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