Pattern reinstatement and attentional control overlap during episodic long-term memory retrieval

Abstract

Episodic long-term memory (eLTM) retrieval involves the reinstatement of neural patterns from the encoding phase. However, recent evidence suggests that comparable cortical activity patterns can also be linked to attentional control processes on the level of memory representations. The current investigation assesses these two processes independently based on alpha-beta-band activity in the electroencephalogram (EEG). During encoding, subjects were presented with an object on a certain position on the screen and had to imagine it on a new position. In each trial, either the task-irrelevant presentation position or the task-relevant imagination position was lateralized. In the retrieval phase, subjects first made an old/new judgement based on centrally presented objects and then reported the imagination position. Pattern reinstatement should be reflected in similar lateralized alpha-beta activity during encoding and retrieval. Conversely, the influence of attentional control processes during retrieval would be associated with the suppression of alpha-beta power contralateral to the to-be-reported imagination position and with the increase of activity contralateral to the irrelevant presentation position. Our results support this latter pattern. This shows that an experimental differentiation between selective attention and pattern reinstatement processes is necessary when studying the neural basis of eLTM retrieval.

Figure 1

Schematic illustration of the experimental procedure. In the encoding phase, subjects were required to learn associations between everyday objects and imagination positions (top, bottom, left or right). Each object was presented three times during the encoding phase and was supposed to be associated with the same imagination position. In the retrieval phase, subjects completed first an old/new recognition task, in which objects from the previous phase were randomly interleaved with a set of 120 previously unseen objects. If participants reported being familiar with the respective item, they were asked to report the associated imagination position. At the end of each trial, an inter-trial interval (ITI) randomly varying between 1000 and 1500 ms (encoding phase) or 500–1000 ms (retrieval phase) was introduced.

Figure 2

Schematic illustration of the hypotheses. Based on previous research^,, we expect to find a contralateral alpha-beta decrease with respect to both the presentation position, as well as to the imagination position in the encoding phase. As for the retrieval phase, two alternative hypotheses were formulated. If lateralized alpha-beta-band activity reflects pattern reinstatement, a contralateral alpha-beta decrease is expected both with respect to the presentation and to the imagination position. However, if alpha-beta oscillations reflect attentional selection mechanisms, a contralateral alpha-beta increase with respect to the task-irrelevant information and a decrease with respect to the task-relevant information is expected.

Figure 3

Behavioral performance. a. Boxplot illustrating the distribution of average accuracy (%) for the old/new recognition and imagination position recall task. All participants show above-chance performance (chance level recognition task: 50%; recall task: 25%). b. Boxplot showing the distribution of average reaction times (ms) for the two tasks: M_recognition = 1538.80 ms, SD_recognition= 102.70 ms; M_recall = 1364.10 ms, SD_recall = 199.25 ms. c. Boxplot illustrating the distribution of incorrect responses. The Y-axis denotes the frequency of reporting the respective incorrect position, where the maximum value is 30.

Figure 4

Line plot: lateralized posterior alpha-beta analysis. Data were obtained from a posterior electrode cluster: TP7/8, P5/6, P7/8, PO7/8. The shaded area represents the standard error of the mean activity. a. Time course of the contralateral and ipsilateral alpha-beta power (8–20 Hz) during the encoding phase, with respect to presentation position (left) and imagination postion (right). The gray area marks the significant cluster (p < .05) obtained as a results of the cluster-based permutation procedure used to contrast the contralateral an ipsilateral activity (time window: 0–2582 ms). b. Time course of the contralateral and ipsilateral alpha-beta power (8–20 Hz) during retrieval phase, with respect to the presentation position (left) and the imagination postion (right). c. Comparison of the contralateral-minus-ipsilateral alpha-beta power between the two conditions of the retrieval phase (i.e., relative to the presentation and imagination positions). The gray area marks the significant cluster (p < .05) obtained as a results of the cluster-based permutation procedure. The procedure was conducted on the 0–1250 ms time window, as indicated by the gray dotted lines. d. Time course of the contralateral-minus-ipsilateral power averaged for the two conditions of the retrieval phase. The cluster-based permutation procedure was conducted on the 0–1250 ms time window, as indicated by the gray dotted lines.

Figure 5

Laterlized alpha-beta analysis. a, b, c, d. The left panel depicts the time–frequency representation of the contralateral, ipsilateral, and contralateral-minus-ipsilateral data for the two phases (encoding and retrieval) and relative to the two positions (presentation and imagination). The activity-of-intereset was obtained from a posterior electrode cluster: TP7/8, P5/6, P7/8, PO7/8. Dotted lines indicate the frequencies of interest (8–20 Hz). The right panel shows the topographical distribution of the contralateral-minus-ipsilateral alpha-beta activity.

Figure 6

Results of the ERP analysis–encoding phase. The shaded area represents the standard error of the mean activity. a. Time course of the contralateral, ipsilateral, and contralateral-minus-ipsilateral frontal ERP activity during the encoding phase, with respect to presentation position (left) and imagination postion (right). The contralateral and ipsilateral activity was contrasted using a cluster-based permutation approach for the time-window: 0–2500 ms, as indicated by the dotted lines. The significant clusters are marked with gray. b. Time course of the contralateral, ipsilateral, and contralateral-minus-ipsilateral posterior ERP activity during the encoding phase, with respect to presentation position (left) and imagination postion (right). The contralateral and ipsilateral activity was contrasted using a cluster-based permutation approach for the time-window: 0–2500 ms, as indicated by the dotted lines. The significant clusters are marked with gray. c. Time course of the topographical distribution of the contralateral-minus-ipsilateral ERP activity relative to the imagination position.

Figure 7

Results of the ERP analysis–retrieval phase. The shaded area represents the standard error of the mean activity. a. Time course of the contralateral, ipsilateral, and contralateral-minus-ipsilateral frontal ERP activity relative to the presentation position (left) and to the imagination position (middle). The right panel depicts the comparison of the frontal contralateral-minus-ipsilateral ERP activity between the two conditions. The gray area marks the significant cluster (p < .05) obtained as a results of the cluster-based permutation procedure. The statistical testing was conducted separately for two time windows: 0–1250 ms and 1250–2500 ms, as indicated by the gray dotted lines. b. Time course of the contralateral, ipsilateral, and contralateral-minus-ipsilateral posterior ERP activity relative to the presentation position (left) and to the imagination position (middle). The right panel depicts the comparison of the posterior contralateral-minus-ipsilateral ERP activity between the two conditions. The gray area marks the significant cluster (p < .05) obtained as a results of the cluster-based permutation procedure. The statistical testing was conducted separately for two time windows: 0–1250 ms and 1250–2500 ms, as indicated by the gray dotted lines.

Figure 8

Results of brain-behavior correlations. a. Spearman’s correlation coefficient depicting the correlation between the average contralateral-minus-ipsilateral alpha-beta activity and frontal lateralized ERP effects (the ERP lateralization at channels F9/F10). The gray area reflects the significant cluster (p < .05) obtained as a result of the cluster-based permutation approach. b. Scatterplot of the negative correlation between the two parameters of interest averaged over the significant cluster.