Elsevier

NeuroImage

Volume 29, Issue 4, 15 February 2006, Pages 1117-1126
NeuroImage

Differential effects of distraction during working memory on delay-period activity in the prefrontal cortex and the visual association cortex

https://doi.org/10.1016/j.neuroimage.2005.08.024Get rights and content

Abstract

Maintaining relevant information for later use is a critical aspect of working memory (WM). The lateral prefrontal cortex (PFC) and posterior sensory cortical areas appear to be important in supporting maintenance. However, the relative and unique contributions of these areas remain unclear. We have designed a WM paradigm with distraction to probe the contents of maintenance representations in these regions. During delayed recognition trials of faces, selective interference was evident behaviorally with face distraction leading to significantly worse performance than with scene distraction. Event-related fMRI of the human brain showed that maintenance activity in the lateral PFC, but not in visual association cortex (VAC), was selectively disrupted by face distraction. Additionally, the functional connectivity between the lateral PFC and the VAC was perturbed during these trials. We propose a hierarchical and distributed model of active maintenance in which the lateral PFC codes for abstracted mnemonic information, while sensory areas represent specific features of the memoranda. Furthermore, persistent coactivation between the PFC and sensory areas may be a mechanism by which information is actively maintained.

Introduction

Working memory (WM) is a complex process and is composed of multiple component cognitive processes. A cardinal feature of WM is the on-line maintenance of information to guide future behavior. The specification of the functional neuro-architecture subserving this process remains controversial. In tasks involving visual objects, one group of studies points to the lateral prefrontal cortex (PFC) (Courtney et al., 1997, Courtney et al., 1998, Funahashi et al., 1989, Fuster, 1973, McCarthy et al., 1996, Miller et al., 1996, Scalaidhe et al., 1999) as the site of maintenance, while others implicate the visual association cortex (VAC) (Druzgal and D'Esposito, 2003, Postle and D'Esposito, 1999, Postle et al., 2003, Ranganath et al., 2004). Additionally, few studies have provided clear evidence for the nature of the representations coded by persistent delay period activity.

In the field of cognitive psychology, distraction paradigms have been instrumental in lending empirical support to influential models of WM (Baddeley et al., 1984, Logie et al., 1990). These paradigms rely on the logic that a distractor disrupts WM performance by engaging and interfering with a capacity-limited pathway that is common to distraction and WM processing. Monkey electrophysiology and human fMRI experiments have adopted delayed response paradigms with distraction to identify neural pathways subserving maintenance. They are based on the rationale that only regions whose activity persists after distraction can support maintenance during successful trials. This strategy has been employed to identify distinct regions thought to represent maintenance of verbal (Gruber, 2001) and visual information (Postle et al., 2003) in humans. Single unit studies investigating visual object maintenance have demonstrated delay period activity in the PFC (Fuster, 1973, Scalaidhe et al., 1999) and in IT (Miyashita and Chang, 1988, Nakamura and Kubota, 1995, Sakai and Miyashita, 1991); but only PFC activity has been shown to be resistant to task irrelevant distraction (Miller et al., 1993, Miller et al., 1996). Thus, IT activity may reflect bottom-up, perceptually-driven processes critical to stimulus representation, while PFC activity may reflect processes necessary for goal-directed behavior.

In our human event-related fMRI study, we attempted to clarify the contribution of the lateral PFC and VAC to maintenance by examining delay period activity while subjects performed a delayed response task with distraction. The persistence of delay period activity after distraction implicates that region's involvement in maintenance. To clarify the nature of representations in these areas, we manipulated the congruency of the memoranda and distractor by utilizing two categories of visual objects (faces and scenes) that engage object-specific areas of the PFC (Courtney et al., 1997, Courtney et al., 1998, Sala et al., 2003) and VAC (Epstein and Kanwisher, 1998, Kanwisher et al., 1997). We anticipated that congruency would produce selective interference in WM performance (Jha et al., 2004), which would then allow us to examine the neural correlates of this effect and to make inferences on the nature of representations during maintenance in these areas.

Section snippets

Subjects

Twelve healthy volunteers (ages 23–33; 8 females) participated in this experiment. All participants were recruited from the University of California Berkeley community. This study was approved by the Committee for the Protection of Human Subjects at the University of California Berkeley. All experiments were conducted at the Henry H. Wheeler, Jr. Brain Imaging Center at the University of California Berkeley.

Behavioral paradigm

Stimulus presentation and response recordings were conducted with E-Prime (Psychology

Behavioral data

Mean accuracy and RTs for the face WM task are shown in Fig. 2. Selective interference, e.g. worse performance in the cue/distractor congruent condition, was observed for faces. Face distraction led to greater decrement in accuracy (73.7%) compared to scene distraction (82.4%) (t = 2.64, df = 11, P < 0.05). There was no significant difference in RTs, face/scene = 1242 ms, face/face = 1253 ms (t = 0.54, df = 11, P = 0.60). In the scene WM trials, no congruency effect was observed. Subjects

Discussion

Behaviorally, we observed selective interference between faces. This was manifest as a significant decline in accuracy with face distractors compared to scene distractors during the retention of faces on a delayed response task. While we found sustained activity in the VAC and lateral PFC after distraction, selective interference in the BOLD maintenance signal, greater degradation of activity in the face distraction condition, was evident only in the lateral PFC and not in the VAC. Correlation

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