Multiple gates on working memory

Abstract

The contexts for action may be only transiently visible, accessible, and relevant. The corticobasal ganglia (BG) circuit addresses these demands by allowing the right motor plans to drive action at the right times, via a BG-mediated gate on motor representations. A long-standing hypothesis posits these same circuits are replicated in more rostral brain regions to support gating of cognitive representations. Key evidence now supports the prediction that BG can act as a gate on the input to working memory, as a gate on its output, and as a means of reallocating working memory representations rendered irrelevant by recent events. These discoveries validate key tenets of many computational models, circumscribe motor and cognitive models of recurrent cortical dynamics alone, and identify novel directions for research on the mechanisms of higher-level cognition.

Figure 1

Theoretical overview. (a) All behaving animals must be capable of selecting useful motor actions at the right times. A long-standing hypothesis [11] holds that the same frontostriatal mechanisms supporting this kind of action selection might also support higher-order cognitive functions. (b) Frontostriatal mechanisms can implement a gate to select useful but transient information for rapid storage in working memory, as well as a gate to select of information from working memory to inform motor planning [6,10,13]. (c) Models involving rostral to caudal nesting of corticostriatal input and output gating loops have been shown to solve abstract, multiply contingent action problems [18] as well as forms of Bayesian inference [22^••] and symbolic referencing [23^••]. A key feature of these models is the presence of a ‘diagonal’ rostrocaudal projection (red arrows) allowing rostral areas to modulate the striatal input to more caudal basal ganglia; one implemented model is shown here. (d) Multiple such frontostriatal circuits are thought to exist, each modulated in a top-down manner by more rostral circuits (PMd by pre-PMd; pre-PMd by the inferior frontal sulcus [IFS]; and IFS by the rostrolateral prefrontal cortex [RLPFC]). The diagonal rostrocaudal projections are thought to be particularly important for modulating output gating mechanisms (‘BG out’) as opposed to input gating mechanisms (‘BG in’).

Figure 2

Basal ganglia (BG) contributions to working memory input control. (a) A meta-analysis of over 8000 studies, carried out with Neurosynth’s python package [53], reveals that studies with abstracts including the term ‘updating’ are significantly more likely to report a BOLD response in the bilateral BG (Z = 2.58–7.03, FDR to p < .05; among other regions, not shown). (b) Binding of the competitive dopamine agonist raclopride within the BG is decreased during an updating task (letter memory), relative to a control task (Stroop). (c) Individual differences in D2 binding affinity within the bilateral BG predict individual differences in the rapid updating of working memory (as assessed by the attentional blink), uniquely throughout the brain (even at a liberal threshold of p < .01). (b,c) adapted from [27,29^•] respectively.

Figure 3

Output gating and reallocation. (a) A transient BOLD response is elicited in the dorsal pre-premotor cortex (pre-PMd) by demands on selective output gating. Individual differences in the recruitment of this area and its right hemisphere homologue uniquely predict the mean efficiency of selective output gating, as assessed in behavior. (b) A partially overlapping region also in the vicinity of the pre-PMd shows a differential increase in coupling with the BG during output gating. Individual differences in this coupling uniquely predict behavioral estimates of stochastic variability during selective output gating. (c) BOLD in a more caudal sector of frontal cortex, the PMd, tracks trial to trial changes in the predicted utility of information (as estimated from a reinforcement learning model), but only when it is specified as relevant by a higher-order contextual stimulus. (d) By contrast, when contexts specify information in working memory as irrelevant, predicted utility is differentially tracked by the BOLD response in the bilateral ventral BG. (a,b) Adapted from [48^••]; (c,d) adapted from [50^••].