Biology subjects

Kolling, N.

Publications and source records attributed to Kolling, N..

11 recordsLinked to original sources

bioRxiv2026

Prefrontal mechanisms of goal progress inference and monitoring in macaque monkeys

Primates pursue goals over extended periods and over multiple steps. The ability to track progress and its rate is critical for such pursuit, yet the neural mechanisms of this tracking are unclear. We recorded single-unit activity from macaque midcingulate cortex (MCC) and lateral prefrontal cortex (LPFC) whilst animals worked for immediate rewards and checked a gauge showing progress towards a larger reward. MCC expressed a temporally extended progress rate signal linked to the long timescale neurons in the region. LPFC expressed progress rate only when inferences on that property were required. In MCC, independent feedback-valence information was also preserved, enabling both readout of work success and rate-specific progress updating. An RNN trained under the same constraints showed that progress rate representations emerge spontaneously, and are critical for tracking goal progress. These results demonstrate a frontal mechanism for inferring and predicting goal progress by extracting progress rate information.

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bioRxiv2024

Controllability and cause in human collaboration

There has been considerable interest in how we ascertain whether an environment is controllable and the neural mechanisms mediating this process. An especially acute version of this problem occurs when multiple people collaborate towards a joint outcome. Here we demonstrate that in such ambiguous social contexts, people engage in specific patterns of behaviour that we refer to as active disambiguation. This process helps individuals establish what they themselves, as opposed to others, control and what consequence they themselves cause or that another person causes. People identify when active disambiguation is needed and engage in it at that time. A pattern of activity in the supramarginal gyrus that emerges during and after active disambiguation is linked to establishing controllability and tracking the outcomes from which control is inferred. Activity in this brain region also signals a second learning mechanism, by which individuals attribute outcomes to themselves versus others, in proportion to their perceived control.

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bioRxiv2024

Confidence and insight into working memories are shaped by attention and recent performance

Working memory (WM) is capacity-limited, and our ability to access information from WM is variable, but selective attention to working memory contents can improve performance. People are able to make introspective judgements regarding the quality of their memories, and these judgements are linked to objective memory performance. However, it remains unknown whether benefits of internally directed attention on memory performance occur alongside commensurate changes in introspective judgments. Across two experiments, we used retrospective cues (retro-cues) during working-memory maintenance to direct attention to items in memory. We then examined their consequence on introspective judgements. In the second experiment, we provided trial-wise feedback on performance. We found that selective attention improved confidence judgements and not just performance of the probed item. We were also able to judge participants genuine insight into working-memory contents through the correlation between confidence judgements and memory quality. Neurophysiologically, alpha desynchronization correlated first with memory error and then confidence during retro-cueing, suggesting a sequential process of attentional enhancement of memory contents and introspective insight. Further, we showed that participants can use feedback on the accuracy of confidence judgements to update their beliefs across time, according to performance. Our results emphasize flexibility in working memory by showing we can selectively modulate our confidence about its contents based on internally directed attention or objective feedback.

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bioRxiv2024

General mechanisms of task engagement in the primate frontal cortex

Staying engaged with a task is necessary to maintain goal-directed behaviors. Although engagement varies with the specific task at hand it also exhibits continuous, intrinsic fluctuations widely. This intrinsic component of engagement is difficult to isolate behaviorally or neurally in controlled experiments with humans. By contrast, animals spontaneously move between periods of complete task engagement and disengagement, even in experimental settings. We, therefore, looked at behavior in macaques in a series of four tasks while recording fMRI signals. We identified consistent autocorrelation in task disengagement. This made it possible to build models capturing task-independent engagement and to link it to neural activity. Across all tasks, we identified common patterns of neural activity linked to impending task disengagement in mid-cingulate gyrus. By contrast, activity centered in perigenual anterior cingulate cortex (pgACC) was associated with maintenance of task performance. Importantly, we were able to carefully control for task-specific factors such as the reward history, choice value, and other motivational effects, such as response vigor, as indexed by response time, when identifying neural activity associated with task engagement. Moreover, we showed pgACC activity had a causal link to task engagement; in one of our tasks, transcranial ultrasound stimulation of pgACC, but not of control regions, changed task engagement/disengagement patterns.

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bioRxiv2023

VmPFC supports persistence during goal pursuit through selective attention

Striking the balance between persistence with a goal and flexibility in the face of better options is critical for effectively organizing behaviour across time. While people are often biased towards completing their current goal (e.g. sunk cost biases), it is unclear how these biases occur at a mechanistic level, still allowing for some flexibility for goal abandonment. We propose that ventromedial prefrontal cortex (vmPFC) plays a critical role in orienting attention towards a current goal, prioritising goal completion but allowing for abandonment, particularly when the current goal fails. We developed a novel incremental goal pursuit task to study goal-directed attention and action in healthy individuals with functional magnetic resonance imaging (fMRI), and in an independent group of individuals with brain lesions. The task required participants to make sequential decisions between continuing to persist with a current goal (commitment), versus abandoning progress for a better alternative goal (flexibility). We show that individuals who persist more show greater goal-oriented attention outside the decision period. Increasing attentional capture by the current goal is also revealed in decision-making: people remain more likely to abandon from frustration (collapse of value of the current goal) than from temptation (attraction from valuable alternative goals). Strikingly, we find that our stable inter-individual metrics of persistence and goal-oriented attention were both predicted by baseline activity in vmPFC, tracking goal progress. We present converging evidence from an independent lesion patient study demonstrating the causal involvement of vmPFC in goal persistence: damage to the vmPFC reduces biases to over-persist with the current goal, leading to a performance benefit in our task.

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bioRxiv2022

Strategic exploration in the macaque prefrontal cortex

Humans have been shown to strategically explore. They can identify situations in which gathering information about distant and uncertain options is beneficial for the future. Because primates rely on scare resources when they forage, they are also thought to strategically explore, but whether they use the same strategies as humans and the neural bases of strategic exploration in monkeys are largely unknown. We designed a sequential choice task to investigate whether monkeys mobilize strategic exploration based on whether that information can improve subsequent choice, but also to ask the novel question about whether monkeys adjust their exploratory choices based on the contingency between choice and information, by sometimes providing the counterfactual feedback, about the option not chosen. We show that monkeys decreased their reliance on expected value when exploration could be beneficial, but this was not mediated by changes in the effect of uncertainty on choices. We found strategic exploratory signals in anterior and mid-cingulate cortex (ACC/MCC) and dorsolateral prefrontal cortex (dlPFC). This network was most active when a low value option was chosen which suggests a role in counteracting expected value signals, when exploration away from value should to be considered. Such strategic exploration was abolished when the counterfactual feedback was available. Learning from counterfactual outcome was associated with the recruitment of a different circuit centered on the medial orbitofrontal cortex (OFC), where we showed that monkeys represent chosen and unchosen reward prediction errors. Overall, our study shows how ACC/MCC-dlPFC and OFC circuits together could support exploitation of available information to the fullest and drive behavior towards finding more information through exploration when it is beneficial.

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bioRxiv2021

Spatiotemporally Resolved Multivariate Pattern Analysis for M/EEG

An emerging goal in neuroscience is tracking what information is represented in brain activity over time as a participant completes some task. Whilst EEG and MEG offer millisecond temporal resolution of how activity patterns emerge and evolve, standard decoding methods present significant barriers to interpretability as they obscure the underlying spatial and temporal activity patterns. We instead propose the use of a generative encoding model framework that simultaneously infers the multivariate spatial patterns of activity and the variable timing at which these patterns emerge on individual trials. An encoding model inversion allows predictions to be made about unseen test data in the same way as in standard decoding methodology. These SpatioTemporally Resolved MVPA (STRM) models can be flexibly applied to a wide variety of experimental paradigms, including classification and regression tasks. We show that these models provide insightful maps of the activity driving predictive accuracy metrics; demonstrate behaviourally meaningful variation in the timing of pattern emergence on individual trials; and achieve predictive accuracies that are either equivalent or surpass those achieved by more widely used methods. This provides a new avenue for investigating the brains representational dynamics and could ultimately support more flexible experimental designs in future. HIGHLIGHTSO_LIWe introduce SpatioTemporally Resolved MVPA (STRM), an approach that explicitly models how successive stages of stimulus processing are distributed in both space and time in M/EEG data. C_LIO_LIWe show that STRM is broadly applicable to diverse types of M/EEG data and outputs meaningful and interpretable maps of how neural representations evolve in space and time at millisecond resolution. C_LIO_LIThe trial-specific deviations in activity pattern timings identified by STRM are not random, but vary systematically with inter-trial differences in behavioural, cognitive and physiological variables. C_LIO_LIThese methods result in predictive accuracy metrics that are mostly equivalent to, or a modest improvement on, conventional methods. C_LI

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bioRxiv2020

Temporal Scaling of Human Scalp-Recorded Potentials During Interval Estimation

Much of human behaviour is governed by common processes that unfold over varying timescales. Standard event-related potential analysis assumes fixed-duration responses relative to experimental events. However, recent single unit recordings in animals have revealed neural activity scales to span different durations during behaviours demanding flexible timing. Here, we employed a general linear modelling approach using a novel combination of fixed-duration and variable-duration regressors to unmix fixed-time and scaled-time components in human magneto/electroencephalography (M/EEG) data. We use this to reveal consistent temporal scaling of human scalp-recorded potentials across four independent EEG datasets, including interval perception, production, prediction and value-based decision making. Between-trial variation in the temporally scaled response predicts between-trial variation in subject reaction times, demonstrating the relevance of this temporally scaled signal for temporal variation in behaviour. Our results provide a general approach for studying flexibly timed behaviour in the human brain. Significance StatementNeural activity is traditionally thought to occur over fixed time scales. However, recent animal work has suggested that some neural responses occur over varying timescales. We extended this animal result to humans by detecting temporally scaled signals non-invasively at the scalp in four different tasks. Our results suggest that temporal scaling is an important feature of cognitive processes known to unfold over varying timescales.

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bioRxiv2019

Dopamine and motivational state drive dynamics of human decision making

The mesolimbic dopaminergic system exerts a crucial influence on incentive processing. However, the contribution of dopamine in dynamic, ecological situations where reward rates vary, and decisions evolve over time, remains unclear. In such circumstances, current (foreground) reward accrual needs to be compared continuously with potential rewards that could be obtained by travelling elsewhere (background reward rate), in order to determine the opportunity cost of staying versus leaving. We hypothesised that dopamine specifically modulates the influence of background - but not foreground - reward information when making a dynamic comparison of these variables for optimal behaviour. On a novel foraging task based on an ecological account of animal behaviour (marginal value theorem), human participants were required to decide when to leave locations in situations where foreground rewards depleted at different rates, either in rich or poor environments with high or low background rates. In line with theoretical accounts, peoples decisions to move from current locations were independently modulated by both foreground and background reward rates. Pharmacological manipulation of dopamine D2 receptor activity using the agonist cabergoline significantly affected decisions to move on, specifically modulating the effect of background but not foreground rewards rates. In particular, when on cabergoline, people left patches in poor environments much earlier. These results demonstrate a role of dopamine in signalling the opportunity cost of rewards, not value per se. Using this ecologically derived framework we uncover a specific mechanism by which D2 dopamine receptor activity modulates decision-making when foreground and background reward rates are dynamically compared. Significance statementMany decisions, across economic, political and social spheres, involve choices to "leave". Such decisions depend on a continuous comparison of a current locations value, with that of other locations you could move on to. However, how the brain makes such decisions is poorly understood. Here, we developed a computerized task, based around theories of how animals make decisions to move on when foraging for food. Healthy human participants had to decide when to leave collecting financial rewards in a location, and travel to collect rewards elsewhere. Using a pharmacological manipulation, we show that the activity of dopamine in the brain modulates decisions to move on, with people valuing other locations differently depending on their dopaminergic state.

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bioRxiv2018

The macaque anterior cingulate cortex translates counterfactual choice value into actual behavioral change

The neural mechanisms mediating sensory-guided decision making have received considerable attention but animals often pursue behaviors for which there is currently no sensory evidence. Such behaviors are guided by internal representations of choice values that have to be maintained even when these choices are unavailable. We investigated how four macaque monkeys maintained representations of the value of counterfactual choices - choices that could not be taken at the current moment but which could be taken in the future. Using functional magnetic resonance imaging, we found two different patterns of activity co-varying with values of counterfactual choices in a circuit spanning hippocampus, anterior lateral prefrontal cortex, and anterior cingulate cortex (ACC). ACC activity also reflected whether the internal value representations would be translated into actual behavioral change. To establish the causal importance of ACC for this translation process, we used a novel technique, Transcranial Focused Ultrasound Stimulation, to reversibly disrupt ACC activity.

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bioRxiv2017

Simultaneous representation of a spectrum of dynamically changing value estimates during decision making

Decisions are based on value expectations derived from experience. We show that dorsal anterior cingulate cortex and three other brain regions hold multiple representations of choice value based on different time-scales of experience organized in terms of systematic gradients across the cortex. Some parts of each area represent value estimates based on recent reward experience while others represent value estimates based on experience over the longer term. The value estimates within these four brain areas interact with one another according to their temporal scaling. Some aspects of the representations change dynamically as the environment changes. The spectrum of value estimates may act as a flexible selection mechanism for combining experience-derived value information with other aspects of value to allow flexible and adaptive decisions in changing environments.

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