Dopamine Alters the Fidelity of Working Memory Representations according to Attentional Demands

Abstract

Capacity limitations in working memory (WM) necessitate the need to effectively control its contents. Here, we examined the effect of cabergoline, a dopamine D₂ receptor agonist, on WM using a continuous report paradigm that allowed us to assess the fidelity with which items are stored. We assessed recall performance under three different gating conditions: remembering only one item, being cued to remember one target among distractors, and having to remember all items. Cabergoline had differential effects on recall performance according to whether distractors had to be ignored and whether mnemonic resources could be deployed exclusively to the target. Compared with placebo, cabergoline improved mnemonic performance when there were no distractors but significantly reduced performance when distractors were presented in a precue condition. No significant difference in performance was observed under cabergoline when all items had to be remembered. By applying a stochastic model of response selection, we established that the causes of drug-induced changes in performance were due to changes in the precision with which items were stored in WM. However, there was no change in the extent to which distractors were mistaken for targets. Thus, D₂ agonism causes changes in the fidelity of mnemonic representations without altering interference between memoranda.

Figure 1. Potential effects of dopamine on WM.

(A) Many studies that have examined the effect of dopamine on WM have participants use a binary match-to-sample paradigm. (B) Dopamine might modulate the representation of stored information in ways that cannot readily be detected using such methodology. For example, the resolution of the memoranda could be of varying quality or fidelity (fuzzier representations) but still be sufficient to provide a correct response, that is, a “yes” response in A could correspond to very different underlying representations. Binary report measures might fail to detect gradual changes in the fidelity of stored information with alterations in dopaminergic stimulation. Dopamine does not have to impact on WM in an all-or-nothing manner. (C) An alternative modulatory effect of dopamine might be on interference between the different memoranda, rather than on the quality with which their features are retained. In this scenario, the fidelity of a mental representation may be unaffected, but the features that make up the items may become confused (swapped) during the transition from perception to memory. For example, although the star was perceived as being orange, it is remembered as having the color of the other item (blue).

Figure 2. WM tasks.

(A) One-item task: Participants had to maintain the orientation of one item for a variable duration of time before being probed to reproduce its orientation using a response dial, thereby providing a continuous measure of report on an analog scale. (B) Cued task: Participants were asked to retain only the orientation of the precued item (in this case, pink), which was the same color throughout a block. (C) Uncued task: Participants were asked to keep in mind all four oriented bars and were asked about one of these at response phase.

Figure 3. Absolute angular error.

(A) Comparison of absolute mean angular error for the one-item and cued conditions split according to drug sessions. (B) Comparison of absolute mean angular error for cued and uncued conditions. Error bars reflect within-participant error (standard error of the difference between placebo and drug sessions).

Figure 4. Details of performance in the three tasks on and off cabergoline.

(A) Mean error according to retention delay in the one-item task. Performance according to serial position of probed item in the precued (B) and uncued (C) tasks. There was no interaction between drug and delay duration or serial position. Error bars reflect SEM.

Figure 5. Modeling results for the placebo and cabergoline sessions.

(A) Error can arise in recall because of increased variability in remembering the orientations of the probed item, which is captured in the model in terms of the parameter (kappa). A high kappa corresponds to lower variability in the precision of retained items (for targets or nontargets). Error is also expected to arise through random guessing/responses. Performance on the task not only requires an ability to accurately remember the orientations of bars but also the ability to bind, or associate, an orientation to a specific color. Thus, errors could arise through misbinding remembered orientations with remembered colors. For example, if the pink bar appeared at an orientation of 40° and the cyan bar appeared at 135°, a misbinding error would be said to have occurred if they rotate the probed pink bar to the remembered orientation of the cyan bar. (B) Kappa values according to task and drug. There was a significant difference in kappa on the cued condition and a trend for the one-item condition. (C) Plot showing the relationship between the kappa values for the one-item and precued conditions. (D) Probability of responding to the target (probed item) according to task and drug session. (E) Probability of random guessing according to drug and task. (F) Probability of responding to the distractor (cued task) or nontarget (uncued task) orientation. Error bars reflect the standard error of the difference between placebo and drug sessions.