Elsevier

NeuroImage

Volume 20, Issue 3, November 2003, Pages 1518-1530
NeuroImage

Regular article
Cortical capacity constraints for visual working memory: dissociation of fMRI load effects in a fronto-parietal network

https://doi.org/10.1016/j.neuroimage.2003.07.021Get rights and content

Abstract

Working memory (WM) capacity limitations and their neurophysiological correlates are of special relevance for the understanding of higher cognitive functions. Evidence from behavioral studies suggests that restricted attentional resources contribute to these capacity limitations. In an event-related functional magnetic resonance imaging (fMRI) study, we probed the capacity of the human visual WM system for up to four complex nonnatural objects using a delayed discrimination task. A number of prefrontal and parietal areas bilaterally showed increased blood oxygen level-dependent activity, relative to baseline, throughout the task when more than one object had to be held in memory. Monotonic increases in response to memory load were observed bilaterally in the dorsolateral prefrontal cortex (DLPFC) and the presupplementary motor area (pre-SMA). Conversely, activity in the frontal eye fields (FEFs) and in areas along the intraparietal sulcus (IPS) peaked when subjects had to maintain only two or three objects and decreased in the highest load condition. This dissociation of memory load effects on cortical activity suggests that the cognitive operations subserved by the IPS and FEF, which are most likely related to attention, fail to support visual WM when the capacity limit is approached. The correlation of brain activity with performance implies that only the operations performed by the DLPFC and pre-SMA, which support an integrated representation of visual information, helped subjects to maintain a reasonable level of performance in the highest load condition. These results indicate that at least two distinct cortical subsystems are recruited for visual WM, and that their interplay changes when the capacity limit is reached.

Section snippets

Subjects

All 12 subjects (eight male, four female) were right-handed and had no history of neurological or psychiatric disorder. The mean age was 27.3 years (SD: 2.4 years, age range: 24 to 31 years). All subjects gave written informed consent to participate in the study.

Behavioral task

A delayed visual discrimination task was implemented on a personal computer using custom-developed software (Fig. 1A). Nonnatural objects (BORTS: blurred outlines of random tetris shapes), presented on the center of the computer

Behavioral data

For the behavioral data recorded during the experiment, the ANOVA revealed a significant main effect of memory load on reaction time and accuracy (Fig. 5) (P < 0.05). Accuracy decreased and reaction times increased monotonically with the number of objects. Reaction times were significantly longer for each increase in memory load. Accuracy was significantly lower for memory load 3 and 4 than for memory load 1 and 2. However, even in the highest memory load condition, accuracy was above chance

Discussion

The present study used a paradigm involving the manipulation of the number of non-natural objects that had to be stored in visual WM. We found that activity in the previously described fronto-parietal working memory network was consistently higher in the multiple than in the single object conditions, which conforms to the results of previous fMRI studies Cohen et al., 1997, Jha and McCarthy, 2000. This effect was present at encoding and continued through the entire delay and retrieval period.

Conclusion

By analyzing the cortical BOLD responses associated with increasing memory load, we found evidence for correlates of capacity limitations in visual working memory. We observed dissociation between brain activity patterns in several prefrontal areas, in which activity continued to increase up to the maximum memory load condition of the paradigm, and regions of the visual attention network, in which activity started to decline as the behavioral capacity limit was approached. While these findings

Acknowledgements

J.A.W. is supported by the James S. McDonnell Foundation. The authors thank Harald Mohr, Christoph Bledowski, and Dr. Alexander T. Sack for advice on statistical questions, Dr. Danko Nikolic for valuable comments on the manuscript, and Matthias Bischoff and Pasquale Gagliano for help with data acquisition and analysis. Dr. Francesco Di Salle helped with an earlier version of Fig. 2B. Dr. H. Lanfermann and Professor F.E. Zanella kindly provided access to the MR facilities of the Institute of

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