Differential effects of distraction during working memory on delay-period activity in the prefrontal cortex and the visual association cortex
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
References (58)
- et al.
The variability of human, BOLD hemodynamic responses
NeuroImage
(1998) - et al.
Maintenance versus manipulation of information held in working memory: an event-related fMRI study
Brain Cogn.
(1999) - et al.
Functional interactions between inferotemporal and prefrontal cortex in a cognitive task
Brain Res.
(1985) - et al.
Variation of BOLD hemodynamic responses across subjects and brain regions and their effects on statistical analyses
NeuroImage
(2004) - et al.
Interference with visual short-term memory
Acta Psychol. (Amst.)
(1990) - et al.
Non-spatial memory after selective prefrontal lesions in monkeys
Brain Res.
(1978) Delayed matching after selective prefrontal lesions in monkeys (Macaca mulatta)
Brain Res.
(1975)- et al.
Using event-related fMRI to assess delay-period activity during performance of spatial and nonspatial working memory tasks
Brain Res. Brain Res. Protoc.
(2000) - et al.
Seeking the neural substrates of visual working memory storage
Cortex
(2003) - et al.
Category-specific modulation of inferior temporal activity during working memory encoding and maintenance
Brain Res. Cogn. Brain Res.
(2004)
Measuring functional connectivity during distinct stages of a cognitive task
NeuroImage
The functionally defined right occipital and fusiform “face areas” discriminate novel from visually familiar faces
NeuroImage
Working memory for location and time: activity in prefrontal area 46 relates to selection rather than maintenance in memory
NeuroImage
Functional topography of a distributed neural system for spatial and nonspatial information maintenance in working memory
Neuropsychologia
A trial-based experimental design for fMRI
NeuroImage
Exploring the articulatory loop
Q. J. Exp. Psychol., A
A cortical mechanism for triggering top-down facilitation in visual object recognition
J. Cogn. Neurosci.
Dissociation of working memory from decision making within the human prefrontal cortex
J. Neurosci.
Electrophysiological studies of face perception in humans
J. Cogn. Neurosci.
Contribution of human prefrontal cortex to delay performance
J. Cogn. Neurosci.
Neuronal activity in posterior parietal area 7a during the delay periods of a spatial memory task
J. Neurophysiol.
Transient and sustained activity in a distributed neural system for human working memory
Nature
An area specialized for spatial working memory in human frontal cortex
Science
Neural mechanisms for visual memory and their role in attention
Proc. Natl. Acad. Sci. U. S. A.
Dissecting contributions of prefrontal cortex and fusiform face area to face working memory
J. Cogn. Neurosci.
A cortical representation of the local visual environment
Nature
On the “probable error” of a coefficient of correlation deduced from a small sample
Metron
A comparison of primate prefrontal and inferior temporal cortices during visual categorization
J. Neurosci.
Spatial registration and normalization of images
Hum. Brain Mapp.
Cited by (106)
Neural basis of distractor resistance during visual working memory maintenance
2021, NeuroImageCitation Excerpt :Protection of visual working memory (WM) representations from the interference posed by the incoming task-irrelevant visual input is critically important for efficient WM under real-life conditions. Distractor interference resistance has shown to be particularly challenging when irrelevant distractors match the WM content and there is a substantial overlap in their neural representations (Clapp et al., 2010; Dolcos et al., 2007; Sreenivasan and Jha, 2007; Yoon et al., 2006). In spite of the extensive previous research effort, the neural processes underlying the mitigation of the interference caused by external delay distractors are poorly understood.
Brain circuitry underlying the ABC model of anxiety
2021, Journal of Psychiatric ResearchDistraction in Visual Working Memory: Resistance is Not Futile
2021, Trends in Cognitive SciencesCitation Excerpt :The congruency effect, reflected in both the speed and accuracy of responses, has been replicated extensively at the level of modality (i.e., audio/visual) [21] and it also extends to the category level [22–24]. For example, working memory for faces is more impaired by other face distractors than by scene distractors [24]. A similar relationship is also present for low-level features (e.g., memory for spatial frequency is impaired by distractors differing in spatial frequency but not in orientation) [25,26].