What are the neural mechanisms underlying working memory (WM)? One influential theory posits that neurons in lateral prefrontal cortex (lPFC) store WM information via persistent activity. In this review, we critically evaluate recent findings that together indicate that this model of WM needs revision. We argue that sensory cortex, not lPFC, maintains high-fidelity representations of WM content. In contrast, lPFC simultaneously maintains representations of multiple goal-related variables that serve to bias stimulus-specific activity in sensory regions. This work highlights multiple neural mechanisms supporting WM, including temporally dynamic population coding in addition to persistent activity. These new insights focus the question on understanding how the mechanisms that underlie WM are related, interact, and are coordinated in lPFC and sensory cortices.
Visual working memory (VWM) recruits a broad network of brain regions, including prefrontal, parietal, and visual cortices. Recent evidence supports a "sensory recruitment" model of VWM, whereby precise visual details are maintained in the same stimulus-selective regions responsible for perception. A key question in evaluating the sensory recruitment model is how VWM representations persist through distracting visual input, given that the early visual areas that putatively represent VWM content are susceptible to interference from visual stimulation.To address this question, we used a functional magnetic resonance imaging inverted encoding model approach to quantitatively assess the effect of distractors on VWM representations in early visual cortex and the intraparietal sulcus (IPS), another region previously implicated in the storage of VWM information. This approach allowed us to reconstruct VWM representations for orientation, both before and after visual interference, and to examine whether oriented distractors systematically biased these representations. In our human participants (both male and female), we found that orientation information was maintained simultaneously in early visual areas and IPS in anticipation of possible distraction, and these representations persisted in the absence of distraction. Importantly, early visual representations were susceptible to interference; VWM orientations reconstructed from visual cortex were significantly biased toward distractors, corresponding to a small attractive bias in behavior. In contrast, IPS representations did not show such a bias. These results provide quantitative insight into the effect of interference on VWM representations, and they suggest a dynamic tradeoff between visual and parietal regions that allows flexible adaptation to task demands in service of VWM. Despite considerable evidence that stimulus-selective visual regions maintain precise visual information in working memory, it remains unclear how these representations persist through subsequent input. Here, we used quantitative model-based fMRI analyses to reconstruct the contents of working memory and examine the effects of distracting input. Although representations in the early visual areas were systematically biased by distractors, those in the intraparietal sulcus appeared distractor-resistant. In contrast, early visual representations were most reliable in the absence of distraction. These results demonstrate the dynamic, adaptive nature of visual working memory processes, and provide quantitative insight into the ways in which representations can be affected by interference. Further, they suggest that current models of working memory should be revised to incorporate this flexibility.
Selective attention has been shown to bias sensory processing in favor of relevant stimuli and against irrelevant or distracting stimuli in perceptual tasks. Increasing evidence suggests that selective attention plays an important role during working memory maintenance, possibly by biasing sensory processing in favor of to-be-remembered items. In the current study, we investigated whether selective attention may also support working memory by biasing processing against irrelevant and potentially distracting information. Event-related potentials (ERPs) were recorded while subjects (n = 22) performed a delayed-recognition task for faces and shoes. The delay period was filled with face or shoe distractors. Behavioral performance was impaired when distractors were congruent with the working memory domain (e.g., face distractor during working memory for faces) relative to when distractors were incongruent with the working memory domain (e.g., face distractor during shoe working memory). If attentional biasing against distractor processing is indeed functionally relevant in supporting working memory maintenance, perceptual processing of distractors is predicted to be attenuated when distractors are more behaviorally intrusive relative to when they are nonintrusive. As such, we predicted that perceptual processing of distracting faces, as measured by the face-sensitive N170 ERP component, would be reduced in the context of congruent (face) working memory relative to incongruent (shoe) working memory. The N170 elicited by distracting faces demonstrated reduced amplitude during congruent versus incongruent working memory. These results suggest that perceptual processing of distracting faces may be attenuated due to attentional biasing against sensory processing of distractors that are most behaviorally intrusive during working memory maintenance.
The predominant neurobiological model of working memory (WM) posits that stimulus information is stored via stable elevated activity within highly selective neurons. Based on this model, which we refer to as the canonical model, the storage of stimulus information is largely associated with lateral prefrontal cortex (lPFC). A growing number of studies describe results that cannot be fully explained by the canonical model, suggesting that it is in need of revision. In the present study, we directly test key elements of the canonical model. We analyzed functional MRI data collected as participants performed a task requiring WM for faces and scenes. Multivariate decoding procedures identified patterns of activity containing information about the items maintained in WM (faces, scenes, or both). While information about WM items was identified in extrastriate visual cortex (EC) and lPFC, only EC exhibited a pattern of results consistent with a sensory representation. Information in both regions persisted even in the absence of elevated activity, suggesting that elevated population activity may not represent the storage of information in WM. Additionally, we observed that WM information was distributed across EC neural populations that exhibited a broad range of selectivity for the WM items rather than restricted to highly selective EC populations. Finally, we determined that activity patterns coding for WM information were not stable, but instead varied over the course of a trial, indicating that the neural code for WM information is dynamic rather than static. Together, these findings challenge the canonical model of WM.
Although the contents of working memory (WM) can be decoded from activity in visual cortex, these representations may play a limited role if they are not robust to distraction. Here, we used model-based fMRI to estimate the impact that a distracting visual task had on WM representations in several visual field maps in visual and frontoparietal association cortex. Distraction caused the fidelity of WM representations in all maps to briefly dip when both the memorandum and distractor were jointly encoded by the population activities. Moreover, distraction induced small biases in memory errors which were predicted by biases in neural decoding in early visual cortex, but not other regions. Although distraction briefly disrupts WM representations, the widespread redundancy with which WM information is encoded may protect against catastrophic loss. In early visual cortex, nonetheless, the neural representation of information in WM and behavioral performance were intertwined, solidifying its importance in memory.
Although the contents of working memory can be decoded from visual cortex activity, these representations may play a limited role if they are not robust to distraction. We used model-based fMRI to estimate the impact of distracting visual tasks on working memory representations in several visual field maps in visual and frontoparietal association cortex. Here, we show distraction causes the fidelity of working memory representations to briefly dip when both the memorandum and distractor are jointly encoded by the population activities. Distraction induces small biases in memory errors which can be predicted by biases in neural decoding in early visual cortex, but not other regions. Although distraction briefly disrupts working memory representations, the widespread redundancy with which working memory information is encoded may protect against catastrophic loss. In early visual cortex, the neural representation of information in working memory and behavioral performance are intertwined, solidifying its importance in visual memory.
In the present study, we investigated whether attention to faces results in sensory gain modulation. Participants were cued to attend either to faces or to scenes in superimposed face-scene images for which face discriminability was manipulated parametrically. The face-sensitive N170 event-related potential component was used as a measure of early face processing. Attention to faces modulated N170 amplitude, but only when faces were not highly discriminable. Additionally, directing attention to faces modulated later processing (~230-300 msec) for all discriminability levels. These results demonstrate that attention to faces can modulate perceptual processing of faces at multiple stages of processing, including early sensory levels. Critically, the early attentional benefit is present only when the "face signal" (i.e., the perceptual quality of the face) in the environment is suboptimal.
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