Retrospective cues mitigate information loss in human cortex during working memory storage

Abstract

Working memory (WM) enables the flexible representation of information over short intervals. It is well-established that WM performance can be enhanced by a retrospective cue presented during storage, yet the neural mechanisms responsible for this benefit are unclear. Here, we tested several explanations for retro-cue benefits by quantifying changes in spatial WM representations reconstructed from alpha-band (8-12 Hz) EEG activity recorded from human participants (both sexes) before and after presentation of a retrospective cue. This allowed us to track cue-related changes in WM representations with high temporal resolution (tens of milliseconds). Participants encoded the locations of two colored discs for subsequent report. During neutral trials an uninformative cue instructed participants to remember the locations of both discs across a blank delay, and we observed a monotonic decrease in the fidelity of reconstructed spatial WM representations with time. During valid trials a 100% reliable cue indicated the color of the disc participants would be probed to report. Critically, valid cues were presented immediately after termination of the encoding display (“valid early”, or VE trials) or midway through the delay period (“valid late” or VL trials). During VE trials the gradual loss of location-specific information observed during neutral trials was eliminated, while during VL trials it was partially reversed. Our findings suggest that retro-cues engage several different mechanisms that together serve to mitigate information loss during WM storage.Significance StatementWorking memory (WM) performance can be improved by a cue presented during storage. This effect, termed a retrospective cue benefit, has been used to explore the limitations of attentional prioritization in WM. However, the mechanisms responsible for retrospective cue benefits are unclear. Here we tested several explanations for retrospective cue benefits by examining how they influence WM representations reconstructed from human EEG activity. This approach allowed us to visualize, quantify, and track the effects of retrospective cues with high temporal resolution (on the order of tens of milliseconds). We show that under different circumstances retrospective cues can both eliminate and even partially reverse information loss during WM storage, suggesting that retrospective cue benefits have manifold origins.

Information recovery following a retrospective cue decreases with time

“…In keeping with earlier studies (e.g., Sprague et al, 2016;Wolff et al, 2017), Ester et al (2018) interpreted the partial recovery of location-specific information observed during valid late trials as evidence that participants were able to supplement active memory representations indexed by alpha-band activity with other information sources not indexed by this activity, including but not limited to "activity silent" WM or long-term memory. In this study, we asked whether participants' ability to exploit these additional memory stores is time-dependent.…”

“…If so, then one would expect that the extent of retrocue-driven recovery in estimates of location information would decrease as the temporal interval separating the encoding display and retrocue increases. We tested this possibility by replicating the neutral and VL conditions from Ester et al (2018) while varying the timing of the retrocue between 1.0, 1.5, and 2.0 sec after the encoding display As expected, we found that degree of information recovery was linearly and inversely related to the interval separating the retrocue and the encoding display, suggesting that representations stored in "offline" memory systems degrade or become more difficult to access over time.…”

“…To examine the effects of retro-cues on spatial WM representations, Ester et al (2018) computed an estimate of location-specific information for the cued and non-cued disc locations by applying an inverted encoding model to spatiotemporal patterns of induced alpha-band activity over occipitoparietal electrode sites during the blank delay period (e.g., Foster et al J Neurophysiol 2016). During neutral trials, where no cue was presented, the authors observed a monotonic decrease in location-specific information over the course of the delay period.…”

Categorical Biases in Human Occipitoparietal Cortex

“…Following earlier work (e.g., Foster et al, 2016;Samaha et al, 2016;Ester et al, 2018;Nouri & Ester, 2019), we used spatiotemporal patterns of induced alpha-band (8-12 Hz) activity over occipitoparietal electrode sites to track the contents of spatial working memory during the recall and DMC tasks. Specifically, we modeled sample-by-sample estimates of alpha band activity recorded during the spatial recall task as a combination of 12 location filters, each with an idealized tuning curve (a cosine raised to the 12 th power).…”

“…Experiment 3 relied on a fundamentally different signal than Experiment 2 (induced-alpha-band activity vs. evoked 30 Hz power, respectively). Following earlier research(Kok et al, 2017;Ester et al, 2018;Nouri & Ester, 2019), we used a variant of the IEM approach described in Experiment 2 to compute location channel responses. We first isolated alpha-band activity, by bandpass filtering the raw EEG time series at each electrode from 8-12 Hz (zero-phase forward and reverse filters as implemented by EEGLAB's "eegfilt"…”