Neural mechanisms of proactive interference-resolution
Introduction
Short-term memory plays an integral role in most forms of intelligent behavior. For example, differences in short-term memory capacity are related to differences in IQ, reasoning, reading comprehension, and problem-solving (Daneman and Carpenter, 1980, Carpenter et al., 1990, Daneman and Merikle, 1996, Just and Carpenter, 1999, Cowan et al., 2005). What determines how much information we can hold online at a given time? One powerful factor is the ability to mitigate proactive interference originating from previously relevant, but no longer relevant information (see, e.g., Keppel and Underwood, 1962, Jonides and Nee, 2006). Due to its central importance in understanding short-term memory, the neural mechanisms underlying proactive interference and its resolution have been a topic of intense interest (Jonides et al., 1998, D’Esposito et al., 1999, Jonides et al., 2000, Mecklinger et al., 2003, Nelson et al., 2003, Badre and Wagner, 2005, Jonides and Nee, 2006).
The lion’s share of neural work on proactive interference has focused on variants of a single paradigm, which we shall refer to as the Recent Probes task (Monsell, 1978, Jonides and Nee, 2006). In the Recent Probes task, subjects are given a small set of items (the target set) to remember over a short retention-interval, followed by a recognition probe (Sternberg, 1966). Recognition probes can either be members of the target set (positive probes) or not (negative probes). Additionally, probes can be members of the target set of the previous trial (recent probes) or not (non-recent probes). Crossing these 2 factors produces four types of probes: recent positive, non-recent positive, recent negative, and non-recent negative. What is of interest with this task is that subjects show slowed reaction times and increased error rates when rejecting recent negative probes compared to non-recent negative probes (Monsell, 1978, McElree and Dosher, 1989). This performance decrement is taken to be a marker of proactive interference. Subjects also tend to show faster reaction times and reduced error rates when responding to recent positive probes compared to non-recent positive probes although this facilitation effect is often far more subtle than the interference effect (Jonides and Nee, 2006).
There has been a burgeoning literature of neuroimaging studies examining the neural correlates of the resolution of proactive interference in the Recent Probes task (Jonides et al., 1998, D’Esposito et al., 1999, Jonides et al., 2000, Mecklinger et al., 2003, Nelson et al., 2003, Badre and Wagner, 2005, Jonides and Nee, 2006). These studies have converged on left ventrolateral prefrontal cortex (VLPFC) as a region important in the resolution of proactive interference (see Jonides and Nee, 2006 for a review). Complementing these studies, neuropsychological work has demonstrated that damage to left VLPFC causes vastly increased proactive interference, while relatively sparing other aspects of short-term memory performance (Thompson-Schill et al., 2002, Hamilton and Martin, 2005). Additionally, elderly subjects show reduced activation in this region relative to younger adults concomitant with an increase in susceptibility to proactive interference (Jonides et al., 2000, Thompson-Schill et al., 2002).
Although the role of left VLPFC in resolving proactive interference is well established in the Recent Probes task, there has been relatively little work testing the generality of this effect. Some efforts have demonstrated left VLPFC involvement in proactive interference-resolution in other tasks (Gray et al., 2003, Zhang et al., 2003, Derrfuss et al., 2004, Postle and Brush, 2004). However, when comparing across different groups of subjects and analysis methods, it is difficult to draw strong conclusions. Recognizing this shortcoming, several studies have examined interference-resolution using multiple paradigms in the same subjects (Peterson et al., 2002, Fan et al., 2003, Liu et al., 2004, Wager et al., 2005). However, all of these studies have focused upon interference caused by response conflict or perceptual distraction. By contrast, no study has examined proactive interference-resolution across multiple tasks. This is an important omission since there is evidence that the resolution of proactive interference may be uniquely distinct from other forms of interference-resolution (Friedman and Miyake, 2004). Therefore, to provide more generality to the claim that left VLPFC plays a critical role in proactive interference, it is important to demonstrate that it shows the same pattern of activity within the same set of subjects across different tasks.
Beyond this, the mechanisms by which left VLPFC participates in the resolution of proactive interference are unclear. Jonides and Nee (2006) reviewed several potential models of left VLPFC function in the service of proactive interference-resolution. These models postulate contrasting positions regarding whether left VLPFC is engaged in response selection, episodic retrieval, or biasing of internal representations. Each account relies on left VLPFC being a node in a functional network that overcomes proactive interference. However, each account varies in its prediction about the particular network involved. Therefore, whether left VLPFC is functionally correlated with response-related regions (e.g., the anterior cingulate, premotor cortex), memory-related regions (e.g., medial temporal lobe), or both will inform models of proactive-interference-resolution. To date, no study has examined the functional connectivity of left VLPFC in the face of proactive interference.
A recent study demonstrated that, in the Recent Probes task, the left VLPFC not only showed enhanced activation to recent negative probes compared to non-recent negative probes, but also increased activation to recent positive probes compared to non-recent positive probes (Badre and Wagner, 2005). Behaviorally, whereas recent negative probes in this study led to interference relative to non-recent negative probes, recent positive probes demonstrated facilitation relative to non-recent positive probes. This paradoxical result is difficult to reconcile within current models of left VLPFC function that attempt to lodge both interference and facilitation effects in this one region of cortex (Jonides and Nee, 2006). Therefore, it is of interest to explore regions related to the facilitation effect associated with recent positive probes.
In addition to left VLPFC, a recent study implicated left anterior prefrontal cortex (APFC) in the Recent Probes task (Badre and Wagner, 2005). The authors found that this region had a striking overlap with activations found in episodic recollection (Dobbins and Wagner, 2005). Also, this region was found to correlate negatively with susceptibility to proactive interference. This pattern of results led the authors to speculate that APFC plays a role in monitoring retrieved information in the service of arriving at a correct decision. Although one study examining the Recent Probes task also demonstrated sub-threshold activation in this region (Jonides et al., 1998), there is little other evidence that this region plays a role in proactive interference tasks. Furthermore, although Badre and Wagner (2005) speculated that APFC may interact with left VLPFC to enable proactive interference-resolution, this possibility has yet to be explored. Therefore, the role of left APFC in proactive interference-resolution is a topic needing additional research.
The present study sought to examine the neural regions involved in the resolution of proactive interference. Here, we scanned subjects using event-related functional magnetic resonance imaging (fMRI) while they performed two different proactive interference tasks: a Recent Probes task and a Directed-Forgetting task. Our novel approach of examining the resolution of proactive interference across multiple tasks in the same subjects allows us to explore interference-related regions that are task-independent. Of particular interest are the behaviors of left VLPFC and left APFC across tasks, since these regions have been implicated during proactive interference-resolution in the Recent Probes task. A previous study examining directed-forgetting in short-term memory with fMRI implicated the left VLPFC for resolving interference from lure probes (Zhang et al., 2003). However, it was unclear that the activations overlapped with those found in the Recent Probes task and furthermore, the activation from Zhang et al. (2003) appeared to be somewhat weak, perhaps due to low power (t(7) = 1.85, p = 0.05, one-tailed). To address these concerns, we used a larger set of subjects to increase power and had subjects perform both tasks in alternating scans in order to determine whether there is common left VLPFC activation across tasks, as well as to further explore the role of left APFC in both tasks. In addition, we used functional connectivity analyses to examine whether left VLPFC and left APFC are functionally related in the face of interference and to explore other regions that show functional coupling to resolve proactive interference. This analysis allowed us to provide a critical test of models of proactive interference-resolution. Finally, we examined whether there are identifiably unique neural signatures of behavioral facilitation in the Recent Probes task, hence providing important data to round out models of proactive interference-resolution.
Section snippets
Participants
Twenty-five University of Michigan students (age range 18–24; mean age = 20.2; 11 male) participated in this study. All were right-handed and native English speakers with normal or corrected-to-normal vision. Subjects were health-screened and informed consent was obtained from all participants in accordance with the University of Michigan Institution Review Board. Participants received $40 in compensation for participation, as well as a bonus based on performance. Two subjects failed to maintain
Behavioral results
Reaction times (RT) were calculated for correct trials only. One-way repeated measures ANOVAs were performed by trial-type separately on error rates (ER) and RT data for each task.
The effect of trial-type in the Recent Probes task was significant in ER (F(1,20) = 12.059, p < 0.001) and RT (F(1,20) = 11.997, p < 0.001). A planned t-test contrasting Recent Negative with Non-Recent Negative probes revealed a significant effect of interference in ER (7.6% vs. 2.6%, t(22) = 4.711, p < 0.001) and RT (844.31 ms
Discussion
The present study sought to inform models of proactive interference by examining neural regions responsive to proactive interference across two separate tasks. First, we generalized the finding of interference-related activity in left VLPFC and left APFC across two different proactive interference tasks in the same subjects. Second, we replicated the finding that left VLPFC correlates positively with interference, whereas left APFC correlates negatively. Third, we demonstrated that although
Acknowledgments
This research was supported in part by the National Science Foundation under Grant No. 0520992, by the National Institute of Mental Health under grant MH60655, and by two National Science Foundation Graduate Research Fellowships to the first and third authors.
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