Publications by authors named "Mark G Stokes"

46 Publications

A hierarchy of functional states in working memory.

J Neurosci 2021 Apr 20. Epub 2021 Apr 20.

Department of Experimental Psychology, University of Oxford, UK.

Extensive research has examined how information is maintained in working memory (WM), but it remains unknown how WM is used to guide behaviour. We addressed this question by combining human electrophysiology (50 subjects, male and female) with pattern analyses, cognitive modelling, and a task requiring the prolonged maintenance of two WM items and priority shifts between them. This enabled us to discern neural states coding for memories that were selected to guide the next decision from states coding for concurrently held memories that were maintained for later use; and to examine how these states contribute to WM-based decisions. Selected memories were encoded in a functionally active state. This state was reflected in spontaneous brain activity during the delay period, closely tracked moment-to-moment fluctuations in the quality of evidence integration, and also predicted when memories would interfere with each other. In contrast, concurrently held memories were encoded in a functionally latent state. This state was reflected only in stimulus-evoked brain activity, tracked memory precision at longer time scales, but did not engage with ongoing decision dynamics. Intriguingly, the two functional states were highly flexible, as priority could be dynamically shifted back and forth between memories without degrading their precision. These results delineate a hierarchy of functional states, whereby latent memories supporting general maintenance are transformed into active decision-circuits to guide flexible behaviour.Working memory enables maintenance of information that is no longer available in the environment. Abundant neuroscientific work has examined in the brain working memories are stored, but it remains unknown they are represented and used to guide behaviour. Our study shows that working memories are represented in qualitatively different formats, depending on behavioural priorities. Memories that are selected for guiding behaviour are encoded in an active state that transforms sensory input into decision variables, whereas other concurrently held memories are encoded in a latent state that supports precise maintenance without affecting ongoing cognition. These results dissociate mechanisms supporting memory storage and usage and open the door to reveal not only where memories are stored but also how.
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http://dx.doi.org/10.1523/JNEUROSCI.3104-20.2021DOI Listing
April 2021

Decoding visual colour from scalp electroencephalography measurements.

Neuroimage 2021 Apr 6:118030. Epub 2021 Apr 6.

Department of Experimental Psychology, University of Oxford, Oxford, UK.

Recent advances have made it possible to decode various aspects of visually presented stimuli from patterns of scalp EEG measurements. As of recently, such multivariate methods have been commonly used to decode visual-spatial features such as location, orientation, or spatial frequency. In the current proof-of-principle study, we show that it is also possible to track visual colour processing by using Linear Discriminant Analysis. Building on other recent demonstrations, we show that colour decoding: (1) reflects sensory qualities (as opposed to, for example, verbal labelling) with a prominent contribution from posterior electrodes contralateral to the stimulus, (2) conforms to a parametric coding space, (3) is possible in multi-item displays, and (4) is comparable in magnitude to the decoding of visual stimulus orientation. Through subsampling our data, we also provide an estimate of the approximate number of trials and participants required for robust decoding. Colour decoding opens a relevant new dimension in which to track visual processing using scalp EEG measurements, while bypassing potential confounds associated with decoding approaches that focus on spatial features.
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http://dx.doi.org/10.1016/j.neuroimage.2021.118030DOI Listing
April 2021

Theoretical distinction between functional states in working memory and their corresponding neural states.

Vis cogn 2020 Sep 24;28(5-8):420-432. Epub 2020 Sep 24.

Wellcome Centre for Integrative Neuroimaging and Department of Experimental Psychology, University of Oxford, Oxford, UK.

Working memory (WM) is important for guiding behaviour, but not always for the next possible action. Here we define a WM item that is currently relevant for guiding behaviour as the functionally "active" item; whereas items maintained in WM, but not immediately relevant to behaviour, are defined as functionally "latent". Traditional neurophysiological theories of WM proposed that content is maintained via persistent neural activity (e.g., stable attractors); however, more recent theories have highlighted the potential role for "activity-silent" mechanisms (e.g., short-term synaptic plasticity). Given these somewhat parallel dichotomies, functionally active and latent cognitive states of WM have been associated with storage based on persistent-activity and activity-silent neural mechanisms, respectively. However, in this article we caution against a one-to-one correspondence between functional and activity states. We argue that the principal theoretical requirement for active and latent WM is that the corresponding neural states play qualitatively different functional roles. We consider a number of candidate solutions, and conclude that the neurophysiological mechanisms for functionally active and latent WM items are theoretically independent of the distinction between persistent activity-based and activity-silent forms of WM storage.
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http://dx.doi.org/10.1080/13506285.2020.1825141DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7655036PMC
September 2020

Comparing the prioritization of items and feature-dimensions in visual working memory.

J Vis 2020 08;20(8):25

Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, UK.

Selective attention can be directed not only to external sensory inputs, but also to internal sensory representations held within visual working memory (VWM). To date, this phenomenon has been studied predominantly following retrospective cues directing attention to particular items, or their locations in memory. In addition to item-level attentional prioritization, recent studies have shown that selectively attending to feature dimensions in VWM can also improve memory recall performance. However, no study to date has directly compared item-based and dimension-based attention in VWM, nor their neural bases. Here, we compared the benefits of retrospective cues (retro-cues) that were directed either at a multifeature item or at a feature dimension that was shared between two spatially segregated items. Behavioral results revealed qualitatively similar attentional benefits in both recall accuracy and response time, but also showed that cueing benefits were larger after item cues. Concurrent electroencephalogram measurements further revealed a similar attenuation of posterior alpha oscillations following both item and dimension retro-cues when compared with noninformative, neutral retro-cues. We argue that attention can act flexibly to prioritize the most relevant information-at either the item or the dimension level-to optimize ensuing memory-based task performance, and we discuss the implications of the observed commonalities and differences between item-level and dimension-level prioritization in VWM.
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http://dx.doi.org/10.1167/jov.20.8.25DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7453048PMC
August 2020

Attentional Control in Subclinical Anxiety and Depression: Depression Symptoms Are Associated With Deficits in Target Facilitation, Not Distractor Inhibition.

Front Psychol 2020 22;11:1660. Epub 2020 Jul 22.

Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom.

Mood and anxiety disorders are associated with deficits in attentional control involving emotive and non-emotive stimuli. Current theories focus on impaired attentional inhibition of distracting stimuli in producing these deficits. However, standard attention tasks struggle to separate distractor inhibition from target facilitation. Here, we investigate whether distractor inhibition underlies these deficits using neutral stimuli in a behavioral task specifically designed to tease apart these two attentional processes. Healthy participants performed a four-location Posner cueing paradigm and completed self-report questionnaires measuring depressive symptoms and trait anxiety. Using regression analyses, we found no relationship between distractor inhibition and mood symptoms or trait anxiety. However, we find a relationship between target facilitation and depression. Specifically, higher depressive symptoms were associated with reduced target facilitation in a task-version in which the target location repeated over a block of trials. We suggest this may relate to findings previously linking depression with deficits in predictive coding in clinical populations.
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http://dx.doi.org/10.3389/fpsyg.2020.01660DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7387660PMC
July 2020

Previously Reward-Associated Stimuli Capture Spatial Attention in the Absence of Changes in the Corresponding Sensory Representations as Measured with MEG.

J Neurosci 2020 06 4;40(26):5033-5050. Epub 2020 May 4.

Department of Experimental Psychology, Wellcome Centre for Integrative Neuroimaging, University of Oxford, Oxford, OX1 3UD, United Kingdom

Studies of selective attention typically consider the role of task goals or physical salience, but attention can also be captured by previously reward-associated stimuli, even if they are currently task irrelevant. One theory underlying this value-driven attentional capture (VDAC) is that reward-associated stimulus representations undergo plasticity in sensory cortex, thereby automatically capturing attention during early processing. To test this, we used magnetoencephalography to probe whether stimulus location and identity representations in sensory cortex are modulated by reward learning. We furthermore investigated the time course of these neural effects, and their relationship to behavioral VDAC. Male and female human participants first learned stimulus-reward associations. Next, we measured VDAC in a separate task by presenting these stimuli in the absence of reward contingency and probing their effects on the processing of separate target stimuli presented at different time lags. Using time-resolved multivariate pattern analysis, we found that learned value modulated the spatial selection of previously rewarded stimuli in posterior visual and parietal cortex from ∼260 ms after stimulus onset. This value modulation was related to the strength of participants' behavioral VDAC effect and persisted into subsequent target processing. Importantly, learned value did not influence cortical signatures of early processing (i.e., earlier than ∼200 ms); nor did it influence the decodability of stimulus identity. Our results suggest that VDAC is underpinned by learned value signals that modulate spatial selection throughout posterior visual and parietal cortex. We further suggest that VDAC can occur in the absence of changes in early visual processing in cortex. Attention is our ability to focus on relevant information at the expense of irrelevant information. It can be affected by previously learned but currently irrelevant stimulus-reward associations, a phenomenon termed "value-driven attentional capture" (VDAC). The neural mechanisms underlying VDAC remain unclear. It has been speculated that reward learning induces visual cortical plasticity, which modulates early visual processing to capture attention. Although we find that learned value modulates spatial signals in visual cortical areas, an effect that correlates with VDAC, we find no relevant signatures of changes in early visual processing in cortex.
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http://dx.doi.org/10.1523/JNEUROSCI.1172-19.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7314418PMC
June 2020

One Thing Leads to Another: Anticipating Visual Object Identity Based on Associative-Memory Templates.

J Neurosci 2020 05 13;40(20):4010-4020. Epub 2020 Apr 13.

Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford OX3 7JX, United Kingdom.

Probabilistic associations between stimuli afford memory templates that guide perception through proactive anticipatory mechanisms. A great deal of work has examined the behavioral consequences and human electrophysiological substrates of anticipation following probabilistic memory cues that carry spatial or temporal information to guide perception. However, less is understood about the electrophysiological substrates linked to anticipating the sensory content of events based on recurring associations between successive events. Here, we demonstrate behavioral and electrophysiological signatures of using associative-memory templates to guide perception, while equating spatial and temporal anticipation (experiments 1 and 2), as well as target probability and response demands (experiment 2). By recording the electroencephalogram in the two experiments ( = 55; 24 females), we show that two markers in human electrophysiology implicated in spatial and temporal anticipation also contribute to the anticipation of perceptual identity, as follows: attenuation of alpha-band oscillations and the contingent negative variation (CNV). Together, our results show that memory-guided identity templates proactively impact perception and are associated with anticipatory states of attenuated alpha oscillations and the CNV. Furthermore, by isolating object-identity anticipation from spatial and temporal anticipation, our results suggest a role for alpha attenuation and the CNV in specific visual content anticipation beyond general changes in neural excitability or readiness. Probabilistic associations between stimuli afford memory templates that guide perception through proactive anticipatory mechanisms. The current work isolates the behavioral benefits and electrophysiological signatures of memory-guided identity-based anticipation, while equating anticipation of space, time, motor responses, and task relevance. Our results show that anticipation of the specific identity of a forthcoming percept impacts performance and is associated with states of attenuated alpha oscillations and the contingent negative variation, extending previous work implicating these neural substrates in spatial and temporal preparatory attention. Together, this work bridges fields of attention, memory, and perception, providing new insights into the neural mechanisms that support complex attentional templates.
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http://dx.doi.org/10.1523/JNEUROSCI.2751-19.2020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7219293PMC
May 2020

Drifting codes within a stable coding scheme for working memory.

PLoS Biol 2020 03 2;18(3):e3000625. Epub 2020 Mar 2.

Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom.

Working memory (WM) is important to maintain information over short time periods to provide some stability in a constantly changing environment. However, brain activity is inherently dynamic, raising a challenge for maintaining stable mental states. To investigate the relationship between WM stability and neural dynamics, we used electroencephalography to measure the neural response to impulse stimuli during a WM delay. Multivariate pattern analysis revealed representations were both stable and dynamic: there was a clear difference in neural states between time-specific impulse responses, reflecting dynamic changes, yet the coding scheme for memorised orientations was stable. This suggests that a stable subcomponent in WM enables stable maintenance within a dynamic system. A stable coding scheme simplifies readout for WM-guided behaviour, whereas the low-dimensional dynamic component could provide additional temporal information. Despite having a stable subspace, WM is clearly not perfect-memory performance still degrades over time. Indeed, we find that even within the stable coding scheme, memories drift during maintenance. When averaged across trials, such drift contributes to the width of the error distribution.
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http://dx.doi.org/10.1371/journal.pbio.3000625DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7067474PMC
March 2020

Unimodal and Bimodal Access to Sensory Working Memories by Auditory and Visual Impulses.

J Neurosci 2020 01 21;40(3):671-681. Epub 2019 Nov 21.

Department of Experimental Psychology, University of Groningen, Groningen, 9712 TS, The Netherlands, and.

It is unclear to what extent sensory processing areas are involved in the maintenance of sensory information in working memory (WM). Previous studies have thus far relied on finding neural activity in the corresponding sensory cortices, neglecting potential activity-silent mechanisms, such as connectivity-dependent encoding. It has recently been found that visual stimulation during visual WM maintenance reveals WM-dependent changes through a bottom-up neural response. Here, we test whether this impulse response is uniquely visual and sensory-specific. Human participants (both sexes) completed visual and auditory WM tasks while electroencephalography was recorded. During the maintenance period, the WM network was perturbed serially with fixed and task-neutral auditory and visual stimuli. We show that a neutral auditory impulse-stimulus presented during the maintenance of a pure tone resulted in a WM-dependent neural response, providing evidence for the auditory counterpart to the visual WM findings reported previously. Interestingly, visual stimulation also resulted in an auditory WM-dependent impulse response, implicating the visual cortex in the maintenance of auditory information, either directly or indirectly, as a pathway to the neural auditory WM representations elsewhere. In contrast, during visual WM maintenance, only the impulse response to visual stimulation was content-specific, suggesting that visual information is maintained in a sensory-specific neural network, separated from auditory processing areas. Working memory is a crucial component of intelligent, adaptive behavior. Our understanding of the neural mechanisms that support it has recently shifted: rather than being dependent on an unbroken chain of neural activity, working memory may rely on transient changes in neuronal connectivity, which can be maintained efficiently in activity-silent brain states. Previous work using a visual impulse stimulus to perturb the memory network has implicated such silent states in the retention of line orientations in visual working memory. Here, we show that auditory working memory similarly retains auditory information. We also observed a sensory-specific impulse response in visual working memory, while auditory memory responded bimodally to both visual and auditory impulses, possibly reflecting visual dominance of working memory.
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http://dx.doi.org/10.1523/JNEUROSCI.1194-19.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6961985PMC
January 2020

Premembering Experience: A Hierarchy of Time-Scales for Proactive Attention.

Neuron 2019 10;104(1):132-146

Department of Experimental Psychology, University of Oxford, Oxford, UK; Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford, UK.

Memories are about the past, but they serve the future. Memory research often emphasizes the former aspect: focusing on the functions that re-constitute (re-member) experience and elucidating the various types of memories and their interrelations, timescales, and neural bases. Here we highlight the prospective nature of memory in guiding selective attention, focusing on functions that use previous experience to anticipate the relevant events about to unfold-to "premember" experience. Memories of various types and timescales play a fundamental role in guiding perception and performance adaptively, proactively, and dynamically. Consonant with this perspective, memories are often recorded according to expected future demands. Using working memory as an example, we consider how mnemonic content is selected and represented for future use. This perspective moves away from the traditional representational account of memory toward a functional account in which forward-looking memory traces are informationally and computationally tuned for interacting with incoming sensory signals to guide adaptive behavior.
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http://dx.doi.org/10.1016/j.neuron.2019.08.030DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6873797PMC
October 2019

Reward Boosts Neural Coding of Task Rules to Optimize Cognitive Flexibility.

J Neurosci 2019 10 13;39(43):8549-8561. Epub 2019 Sep 13.

Department of Experimental Psychology, University of Oxford, Oxford OX2 6AE, United Kingdom, and.

Cognitive flexibility is critical for intelligent behavior. However, its execution is effortful and often suboptimal. Recent work indicates that flexible behavior can be improved by the prospect of reward, which suggests that rewards optimize flexible control processes. Here we investigated how different reward prospects influence neural encoding of task rule information to optimize cognitive flexibility. We applied representational similarity analysis to human electroencephalograms, recorded while female and male participants performed a rule-guided decision-making task. During the task, the prospect of reward varied from trial to trial. Participants made faster, more accurate judgements on high-reward trials. Critically, high reward boosted neural coding of the active task rule, and the extent of this increase was associated with improvements in task performance. Additionally, the effect of high reward on task rule coding was most pronounced on switch trials, where rules were updated relative to the previous trial. These results suggest that reward prospect can promote cognitive performance by strengthening neural coding of task rule information, helping to improve cognitive flexibility during complex behavior. The importance of motivation is evident in the ubiquity with which reward prospect guides adaptive behavior and the striking number of neurological conditions associated with motivational impairments. In this study, we investigated how dynamic changes in motivation, as manipulated through reward, shape neural coding for task rules during a flexible decision-making task. The results of this work suggest that motivation to obtain reward modulates the encoding of task rules needed for flexible behavior. The extent to which reward increased task rule coding also tracked improvements in behavioral performance under high-reward conditions. These findings help to inform how motivation shapes neural processing in the healthy human brain.
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http://dx.doi.org/10.1523/JNEUROSCI.0631-19.2019DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6807286PMC
October 2019

Concurrent visual and motor selection during visual working memory guided action.

Nat Neurosci 2019 03 4;22(3):477-483. Epub 2019 Feb 4.

Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, Oxford, UK.

Visual working memory enables us to hold onto past sensations in anticipation that these may become relevant for guiding future actions. Yet laboratory tasks have treated visual working memories in isolation from their prospective actions and have focused on the mechanisms of memory retention rather than utilization. To understand how visual memories become used for action, we linked individual memory items to particular actions and independently tracked the neural dynamics of visual and motor selection when memories became used for action. This revealed concurrent visual-motor selection, engaging appropriate visual and motor brain areas at the same time. Thus we show that items in visual working memory can invoke multiple, item-specific, action plans that can be accessed together with the visual representations that guide them, affording fast and precise memory-guided behavior.
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http://dx.doi.org/10.1038/s41593-018-0335-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6420070PMC
March 2019

Decoding the influence of anticipatory states on visual perception in the presence of temporal distractors.

Nat Commun 2018 04 13;9(1):1449. Epub 2018 Apr 13.

Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, Warneford Hospital, University of Oxford, Oxford, OX3 7JX, UK.

Anticipatory states help prioritise relevant perceptual targets over competing distractor stimuli and amplify early brain responses to these targets. Here we combine electroencephalography recordings in humans with multivariate stimulus decoding to address whether anticipation also increases the amount of target identity information contained in these responses, and to ask how targets are prioritised over distractors when these compete in time. We show that anticipatory cues not only boost visual target representations, but also delay the interference on these target representations caused by temporally adjacent distractor stimuli-possibly marking a protective window reserved for high-fidelity target processing. Enhanced target decoding and distractor resistance are further predicted by the attenuation of posterior 8-14 Hz alpha oscillations. These findings thus reveal multiple mechanisms by which anticipatory states help prioritise targets from temporally competing distractors, and they highlight the potential of non-invasive multivariate electrophysiology to track cognitive influences on perception in temporally crowded contexts.
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http://dx.doi.org/10.1038/s41467-018-03960-zDOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5899132PMC
April 2018

Selective inhibition of distracting input.

Behav Brain Res 2018 12 16;355:36-47. Epub 2017 Oct 16.

Department of Experimental Psychology, University of Oxford, South Parks Road, Oxford, OX1 3UD, United Kingdom; Oxford Centre for Human Brain Activity, Wellcome Centre for Integrative Neuroimaging, Department of Psychiatry, University of Oxford, OX3 7JX, United Kingdom.

We review a series of studies exploring distractor suppression. It is often assumed that preparatory distractor suppression is controlled via top-down mechanisms of attention akin to those that prepare brain areas for target enhancement. Here, we consider two alternative mechanisms: secondary inhibition and expectation suppression within a predictive coding framework. We draw on behavioural studies, evidence from neuroimaging and some animal studies. We conclude that there is very limited evidence for selective top-down control of preparatory inhibition. By contrast, we argue that distractor suppression often relies secondary inhibition of non-target items (relatively non-selective inhibition) and on statistical regularities of the environment, learned through direct experience.
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http://dx.doi.org/10.1016/j.bbr.2017.10.010DOI Listing
December 2018

Benefits of flexible prioritization in working memory can arise without costs.

J Exp Psychol Hum Percept Perform 2018 Mar 17;44(3):398-411. Epub 2017 Aug 17.

Department of Experimental Psychology, University of Oxford.

Most recent models conceptualize working memory (WM) as a continuous resource, divided up according to task demands. When an increasing number of items need to be remembered, each item receives a smaller chunk of the memory resource. These models predict that the allocation of attention to high-priority WM items during the retention interval should be a zero-sum game: improvements in remembering cued items come at the expense of uncued items because resources are dynamically transferred from uncued to cued representations. The current study provides empirical data challenging this model. Four precision retrocueing WM experiments assessed cued and uncued items on every trial. This permitted a test for trade-off of the memory resource. We found no evidence for trade-offs in memory across trials. Moreover, robust improvements in WM performance for cued items came at little or no cost to uncued items that were probed afterward, thereby increasing the net capacity of WM relative to neutral cueing conditions. An alternative mechanism of prioritization proposes that cued items are transferred into a privileged state within a response-gating bottleneck, in which an item uniquely controls upcoming behavior. We found evidence consistent with this alternative. When an uncued item was probed first, report of its orientation was biased away from the cued orientation to be subsequently reported. We interpret this bias as competition for behavioral control in the output-driving bottleneck. Other items in WM did not bias each other, making this result difficult to explain with a shared resource model. (PsycINFO Database Record
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http://dx.doi.org/10.1037/xhp0000449DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5868459PMC
March 2018

Stable and Dynamic Coding for Working Memory in Primate Prefrontal Cortex.

J Neurosci 2017 07 30;37(27):6503-6516. Epub 2017 May 30.

Department of Experimental Psychology, University of Oxford, Oxford OX1 3UD, United Kingdom.

Working memory (WM) provides the stability necessary for high-level cognition. Influential theories typically assume that WM depends on the persistence of stable neural representations, yet increasing evidence suggests that neural states are highly dynamic. Here we apply multivariate pattern analysis to explore the population dynamics in primate lateral prefrontal cortex (PFC) during three variants of the classic memory-guided saccade task (recorded in four animals). We observed the hallmark of dynamic population coding across key phases of a working memory task: sensory processing, memory encoding, and response execution. Throughout both these dynamic epochs and the memory delay period, however, the neural representational geometry remained stable. We identified two characteristics that jointly explain these dynamics: (1) time-varying changes in the subpopulation of neurons coding for task variables (i.e., dynamic subpopulations); and (2) time-varying selectivity within neurons (i.e., dynamic selectivity). These results indicate that even in a very simple memory-guided saccade task, PFC neurons display complex dynamics to support stable representations for WM. Flexible, intelligent behavior requires the maintenance and manipulation of incoming information over various time spans. For short time spans, this faculty is labeled "working memory" (WM). Dominant models propose that WM is maintained by stable, persistent patterns of neural activity in prefrontal cortex (PFC). However, recent evidence suggests that neural activity in PFC is dynamic, even while the contents of WM remain stably represented. Here, we explored the neural dynamics in PFC during a memory-guided saccade task. We found evidence for dynamic population coding in various task epochs, despite striking stability in the neural representational geometry of WM. Furthermore, we identified two distinct cellular mechanisms that contribute to dynamic population coding.
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http://dx.doi.org/10.1523/JNEUROSCI.3364-16.2017DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5511881PMC
July 2017

Prioritizing Information during Working Memory: Beyond Sustained Internal Attention.

Trends Cogn Sci 2017 06 25;21(6):449-461. Epub 2017 Apr 25.

Oxford Centre for Human Brain Activity, Oxford University, Oxford, UK; Department of Experimental Psychology, Oxford University, Oxford, UK. Electronic address:

Working memory (WM) has limited capacity. This leaves attention with the important role of allowing into storage only the most relevant information. It is increasingly evident that attention is equally crucial for prioritizing representations within WM as the importance of individual items changes. Retrospective prioritization has been proposed to result from a focus of internal attention highlighting one of several representations. Here, we suggest an updated model, in which prioritization acts in multiple steps: first orienting towards and selecting a memory, and then reconfiguring its representational state in the service of upcoming task demands. Reconfiguration sets up an optimized perception-action mapping, obviating the need for sustained attention. This view is consistent with recent literature, makes testable predictions, and links WM with task switching and action preparation.
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http://dx.doi.org/10.1016/j.tics.2017.03.010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7220802PMC
June 2017

Dynamic hidden states underlying working-memory-guided behavior.

Nat Neurosci 2017 Jun 17;20(6):864-871. Epub 2017 Apr 17.

Department of Experimental Psychology, University of Oxford, Oxford, UK.

Recent theoretical models propose that working memory is mediated by rapid transitions in 'activity-silent' neural states (for example, short-term synaptic plasticity). According to the dynamic coding framework, such hidden state transitions flexibly configure memory networks for memory-guided behavior and dissolve them equally fast to allow forgetting. We developed a perturbation approach to measure mnemonic hidden states in an electroencephalogram. By 'pinging' the brain during maintenance, we show that memory-item-specific information is decodable from the impulse response, even in the absence of attention and lingering delay activity. Moreover, hidden memories are remarkably flexible: an instruction cue that directs people to forget one item is sufficient to wipe the corresponding trace from the hidden state. In contrast, temporarily unattended items remain robustly coded in the hidden state, decoupling attentional focus from cue-directed forgetting. Finally, the strength of hidden-state coding predicts the accuracy of working-memory-guided behavior, including memory precision.
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http://dx.doi.org/10.1038/nn.4546DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5446784PMC
June 2017

Distinct Mechanisms for Distractor Suppression and Target Facilitation.

J Neurosci 2016 Feb;36(6):1797-807

Oxford Centre for Human Brain Activity, Department of Psychiatry, University of Oxford, Oxford OX1 3UD, United Kingdom.

Unlabelled: It is well established that preparatory attention improves processing of task-relevant stimuli. Although it is often more important to ignore task-irrelevant stimuli, comparatively little is known about preparatory attentional mechanisms for inhibiting expected distractions. Here, we establish that distractor inhibition is not under the same top-down control as target facilitation. Using a variant of the Posner paradigm, participants were cued to either the location of a target stimulus, the location of a distractor, or were provided no predictive information. In Experiment 1, we found that participants were able to use target-relevant cues to facilitate target processing in both blocked and flexible conditions, but distractor cueing was only effective in the blocked version of the task. In Experiment 2, we replicate these findings in a larger sample and leveraged the additional statistical power to perform individual differences analyses to tease apart potential underlying mechanisms. We found no evidence for a correlation between these two types of benefit, suggesting that flexible target cueing and distractor suppression depend on distinct cognitive mechanisms. In Experiment 3, we use EEG to show that preparatory distractor suppression is associated with a diminished P1, but we found no evidence to suggest that this effect was mediated by top-down control of oscillatory activity in the alpha band (8-12 Hz). We conclude that flexible top-down mechanisms of cognitive control are specialized for target-related attention, whereas distractor suppression only emerges when the predictive information can be derived directly from experience. This is consistent with a predictive coding model of expectation suppression.

Significance Statement: If you were told to ignore a white bear, you might find it quite difficult. Holding something in working memory is thought to automatically facilitate feature processing, even if doing so is detrimental to the current task. Despite this paradox, it is often assumed that distractor suppression is controlled via similar top-down mechanisms of attention that prepare brain areas for target enhancement. In particular, low-frequency oscillations in visual cortex appear especially well suited for gating task-irrelevant information. We describe the results of a series of studies exploring distractor suppression and challenge this popular notion. We draw on behavioral and EEG evidence to show that selective distractor suppression operates via an alternative mechanism, such as expectation suppression within a predictive coding framework.
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http://dx.doi.org/10.1523/JNEUROSCI.2133-15.2016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4748069PMC
February 2016

Testing sensory evidence against mnemonic templates.

Elife 2015 Dec 14;4:e09000. Epub 2015 Dec 14.

Department of Experimental Psychology, University of Oxford, Oxford, United Kingdom.

Most perceptual decisions require comparisons between current input and an internal template. Classic studies propose that templates are encoded in sustained activity of sensory neurons. However, stimulus encoding is itself dynamic, tracing a complex trajectory through activity space. Which part of this trajectory is pre-activated to reflect the template? Here we recorded magneto- and electroencephalography during a visual target-detection task, and used pattern analyses to decode template, stimulus, and decision-variable representation. Our findings ran counter to the dominant model of sustained pre-activation. Instead, template information emerged transiently around stimulus onset and quickly subsided. Cross-generalization between stimulus and template coding, indicating a shared neural representation, occurred only briefly. Our results are compatible with the proposal that template representation relies on a matched filter, transforming input into task-appropriate output. This proposal was consistent with a signed difference response at the perceptual decision stage, which can be explained by a simple neural model.
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http://dx.doi.org/10.7554/eLife.09000DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4755744PMC
December 2015

Decoding Rich Spatial Information with High Temporal Resolution.

Trends Cogn Sci 2015 Nov 1;19(11):636-638. Epub 2015 Oct 1.

Department of Experimental Psychology, University of Oxford, Oxford, UK; Oxford Centre for Human Brain Activity, University of Oxford, Oxford, UK.

New research suggests that magnetoencephalography (MEG) contains rich spatial information for decoding neural states. Even small differences in the angle of neighbouring dipoles generate subtle, but statistically separable field patterns. This implies MEG (and electroencephalography: EEG) is ideal for decoding neural states with high-temporal resolution in the human brain.
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http://dx.doi.org/10.1016/j.tics.2015.08.016DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4636428PMC
November 2015

Revealing hidden states in visual working memory using electroencephalography.

Front Syst Neurosci 2015 3;9:123. Epub 2015 Sep 3.

Oxford Centre for Human Brain Activity, University of Oxford Oxford, UK ; Department of Experimental Psychology, University of Oxford Oxford, UK.

It is often assumed that information in visual working memory (vWM) is maintained via persistent activity. However, recent evidence indicates that information in vWM could be maintained in an effectively "activity-silent" neural state. Silent vWM is consistent with recent cognitive and neural models, but poses an important experimental problem: how can we study these silent states using conventional measures of brain activity? We propose a novel approach that is analogous to echolocation: using a high-contrast visual stimulus, it may be possible to drive brain activity during vWM maintenance and measure the vWM-dependent impulse response. We recorded electroencephalography (EEG) while participants performed a vWM task in which a randomly oriented grating was remembered. Crucially, a high-contrast, task-irrelevant stimulus was shown in the maintenance period in half of the trials. The electrophysiological response from posterior channels was used to decode the orientations of the gratings. While orientations could be decoded during and shortly after stimulus presentation, decoding accuracy dropped back close to baseline in the delay. However, the visual evoked response from the task-irrelevant stimulus resulted in a clear re-emergence in decodability. This result provides important proof-of-concept for a promising and relatively simple approach to decode "activity-silent" vWM content using non-invasive EEG.
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http://dx.doi.org/10.3389/fnsys.2015.00123DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4558475PMC
September 2015

'Activity-silent' working memory in prefrontal cortex: a dynamic coding framework.

Authors:
Mark G Stokes

Trends Cogn Sci 2015 Jul 4;19(7):394-405. Epub 2015 Jun 4.

Oxford Centre for Human Brain Activity, University of Oxford, Oxford, UK. Electronic address:

Working memory (WM) provides the functional backbone to high-level cognition. Maintenance in WM is often assumed to depend on the stationary persistence of neural activity patterns that represent memory content. However, accumulating evidence suggests that persistent delay activity does not always accompany WM maintenance but instead seems to wax and wane as a function of the current task relevance of memoranda. Furthermore, new methods for measuring and analysing population-level patterns show that activity states are highly dynamic. At first glance, these dynamics seem at odds with the very nature of WM. How can we keep a stable thought in mind while brain activity is constantly changing? This review considers how neural dynamics might be functionally important for WM maintenance.
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http://dx.doi.org/10.1016/j.tics.2015.05.004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4509720PMC
July 2015

Temporal dynamics of attention during encoding versus maintenance of working memory: complementary views from event-related potentials and alpha-band oscillations.

J Cogn Neurosci 2015 Mar 22;27(3):492-508. Epub 2014 Sep 22.

University of Oxford.

Working memory (WM) is strongly influenced by attention. In visual WM tasks, recall performance can be improved by an attention-guiding cue presented before encoding (precue) or during maintenance (retrocue). Although precues and retrocues recruit a similar frontoparietal control network, the two are likely to exhibit some processing differences, because precues invite anticipation of upcoming information whereas retrocues may guide prioritization, protection, and selection of information already in mind. Here we explored the behavioral and electrophysiological differences between precueing and retrocueing in a new visual WM task designed to permit a direct comparison between cueing conditions. We found marked differences in ERP profiles between the precue and retrocue conditions. In line with precues primarily generating an anticipatory shift of attention toward the location of an upcoming item, we found a robust lateralization in late cue-evoked potentials associated with target anticipation. Retrocues elicited a different pattern of ERPs that was compatible with an early selection mechanism, but not with stimulus anticipation. In contrast to the distinct ERP patterns, alpha-band (8-14 Hz) lateralization was indistinguishable between cue types (reflecting, in both conditions, the location of the cued item). We speculate that, whereas alpha-band lateralization after a precue is likely to enable anticipatory attention, lateralization after a retrocue may instead enable the controlled spatiotopic access to recently encoded visual information.
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http://dx.doi.org/10.1162/jocn_a_00727DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4678590PMC
March 2015

Preferential encoding of behaviorally relevant predictions revealed by EEG.

Front Hum Neurosci 2014 2;8:687. Epub 2014 Sep 2.

Department of Experimental Psychology, University of Oxford Oxford, UK ; Oxford Centre for Human Brain Activity, University of Oxford Oxford, UK.

Statistical regularities in the environment guide perceptual processing; however, some predictions are bound to be more important than others. In this electroencephalogram (EEG) study, we test how task relevance influences the way predictions are learned from the statistics of visual input, and exploited for behavior. We developed a novel task in which participants are simply instructed to respond to a designated target stimulus embedded in a serial stream of non-target stimuli. Presentation probabilities were manipulated such that a designated target cue stimulus predicted the target onset with 70% validity. We also included a corresponding control contingency: a pre-designated control cue predicted a specific non-target stimulus with 70% validity. Participants were not informed about these contingencies. This design allowed us to examine the neural response to task-relevant predictive (cue) and predicted stimuli (target), relative to task-irrelevant predictive (control cue) and predicted stimuli (control non-target). The behavioral results confirmed that participants learned and exploited task-relevant predictions even when not explicitly defined. The EEG results further showed that target-relevant predictions are coded more strongly than statistically equivalent regularities between non-target stimuli. There was a robust modulation of the response for predicted targets associated with learning, enhancing the response to cued stimuli just after 200 ms post-stimulus in central and posterior electrodes, but no corresponding effects for predicted non-target stimuli. These effects of target prediction were preceded by a sustained frontal negativity following presentation of the predictive cue stimulus. These results show that task relevance critically influences how the brain extracts predictive structure from the environment, and exploits these regularities for optimized behavior.
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http://dx.doi.org/10.3389/fnhum.2014.00687DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4151094PMC
September 2014

Resting GABA and glutamate concentrations do not predict visual gamma frequency or amplitude.

Proc Natl Acad Sci U S A 2014 Jun 9;111(25):9301-6. Epub 2014 Jun 9.

Oxford Centre for Human Brain Activity, Warneford Hospital, University of Oxford, Oxford OX3 7JX, United Kingdom;

Gamma band oscillations arise in neuronal networks of interconnected GABAergic interneurons and excitatory pyramidal cells. A previous study found a correlation between visual gamma peak frequency, as measured with magnetoencephalography, and resting GABA levels, as measured with magnetic resonance spectroscopy (MRS), in 12 healthy volunteers. If true, this would allow studies in clinical populations testing modulation of this relationship, but this finding has not been replicated. We addressed this important question by measuring gamma oscillations and GABA, as well as glutamate, in 50 healthy volunteers. Visual gamma activity was evoked using an established gratings paradigm, and we applied a beamformer spatial filtering technique to extract source-reconstructed gamma peak frequency and amplitude from the occipital lobe. We determined gamma peak frequency and amplitude from the location with maximal activation and from the location of the MRS voxel to assess the relationship of GABA with gamma. Gamma peak frequency was estimated from the highest value of the raw spectra and by a Gaussian fit to the spectra. MRS data were acquired from occipital cortex. We did not replicate the previously found correlation between gamma peak frequency and GABA concentration. Calculation of a Bayes factor provided strong evidence in favor of the null hypothesis. We also did not find a correlation between gamma activity and glutamate or between gamma and the ratio of GABA/glutamate. Our results suggest that cortical gamma oscillations do not have a consistent, demonstrable relationship to excitatory/inhibitory network activity as proxied by MRS measurements of GABA and glutamate.
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http://dx.doi.org/10.1073/pnas.1321072111DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4078853PMC
June 2014

Oscillatory brain state predicts variability in working memory.

J Neurosci 2014 Jun;34(23):7735-43

Department of Experimental Psychology and, Oxford Centre for Human Brain Activity, University of Oxford, Oxford OX1 3UD, United Kingdom.

Our capacity to remember and manipulate objects in working memory (WM) is severely limited. However, this capacity limitation is unlikely to be fixed because behavioral models indicate variability from trial to trial. We investigated whether fluctuations in neural excitability at stimulus encoding, as indexed by low-frequency oscillations (in the alpha band, 8-14 Hz), contribute to this variability. Specifically, we hypothesized that the spontaneous state of alpha band activity would correlate with trial-by-trial fluctuations in visual WM. Electroencephalography recorded from human observers during a visual WM task revealed that the prestimulus desynchronization of alpha oscillations predicts the accuracy of memory recall on a trial-by-trial basis. A model-based analysis indicated that this effect arises from a modulation in the precision of memorized items, but not the likelihood of remembering them (the recall rate). The phase of posterior alpha oscillations preceding the memorized item also predicted memory accuracy. Based on correlations between prestimulus alpha levels and stimulus-related visual evoked responses, we speculate that the prestimulus state of the visual system prefigures a cascade of state-dependent processes, ultimately affecting WM-guided behavior. Overall, our results indicate that spontaneous changes in cortical excitability can have profound consequences for higher visual cognition.
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http://dx.doi.org/10.1523/JNEUROSCI.4741-13.2014DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4044240PMC
June 2014

Aberrant functional connectivity in dissociable hippocampal networks is associated with deficits in memory.

J Neurosci 2014 Apr;34(14):4920-8

FMRIB Centre, University of Oxford, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, Oxford Epilepsy Research Group, Nuffield Department of Clinical Neurosciences, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom, Oxford Centre for Human Brain Activity, University of Oxford, Warneford Hospital, Oxford OX3 7JX, United Kingdom, and Russell Cairns Unit and Departments of Neurosurgery and Neurology, John Radcliffe Hospital, Oxford OX3 9DU, United Kingdom.

In the healthy human brain, evidence for dissociable memory networks along the anterior-posterior axis of the hippocampus suggests that this structure may not function as a unitary entity. Failure to consider these functional divisions may explain diverging results among studies of memory adaptation in disease. Using task-based and resting functional MRI, we show that chronic seizures disrupting the anterior medial temporal lobe (MTL) preserve anterior and posterior hippocampal-cortical dissociations, but alter signaling between these and other key brain regions. During performance of a memory encoding task, we found reduced neural activity in human patients with unilateral temporal lobe epilepsy relative to age-matched healthy controls, but no upregulation of fMRI signal in unaffected hippocampal subregions. Instead, patients showed aberrant resting fMRI connectivity within anterior and posterior hippocampal-cortical networks, which was associated with memory decline, distinguishing memory-intact from memory-impaired patients. Our results highlight a critical role for intact hippocampo-cortical functional communication in memory and provide evidence that chronic injury-induced functional reorganization in the diseased MTL is behavioral inefficient.
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http://dx.doi.org/10.1523/JNEUROSCI.4281-13.2014DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3972719PMC
April 2014

Attention biases visual activity in visual short-term memory.

J Cogn Neurosci 2014 Jul 23;26(7):1377-89. Epub 2014 Jan 23.

University of Oxford.

In the current study, we tested whether representations in visual STM (VSTM) can be biased via top-down attentional modulation of visual activity in retinotopically specific locations. We manipulated attention using retrospective cues presented during the retention interval of a VSTM task. Retrospective cues triggered activity in a large-scale network implicated in attentional control and led to retinotopically specific modulation of activity in early visual areas V1-V4. Importantly, shifts of attention during VSTM maintenance were associated with changes in functional connectivity between pFC and retinotopic regions within V4. Our findings provide new insights into top-down control mechanisms that modulate VSTM representations for flexible and goal-directed maintenance of the most relevant memoranda.
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http://dx.doi.org/10.1162/jocn_a_00577DOI Listing
July 2014

Dynamic coding for cognitive control in prefrontal cortex.

Neuron 2013 Apr 4;78(2):364-75. Epub 2013 Apr 4.

Oxford Centre for Human Brain Activity, University of Oxford, Oxford OX3 7JX, UK.

Cognitive flexibility is fundamental to adaptive intelligent behavior. Prefrontal cortex has long been associated with flexible cognitive function, but the neurophysiological principles that enable prefrontal cells to adapt their response properties according to context-dependent rules remain poorly understood. Here, we use time-resolved population-level neural pattern analyses to explore how context is encoded and maintained in primate prefrontal cortex and used in flexible decision making. We show that an instruction cue triggers a rapid series of state transitions before settling into a stable low-activity state. The postcue state is differentially tuned according to the current task-relevant rule. During decision making, the response to a choice stimulus is characterized by an initial stimulus-specific population response but evolves to different final decision-related states depending on the current rule. These results demonstrate how neural tuning profiles in prefrontal cortex adapt to accommodate changes in behavioral context. Highly flexible tuning could be mediated via short-term synaptic plasticity.
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http://dx.doi.org/10.1016/j.neuron.2013.01.039DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3898895PMC
April 2013