Biology subjects

Holroyd, C. B.

Publications and source records attributed to Holroyd, C. B..

13 recordsLinked to original sources

bioRxiv2026

A Control-Theoretic Account of Cognitive Effort in Working Memory

Cognitive effort is closely linked to prefrontal control, but the control demands imposed by working memory remain poorly understood at the level of neural circuits. We formulated frontoparietal regulation as a feedback-control problem in a conductance-based spiking network comprising an intraparietal ring attractor and a recurrent dorsolateral prefrontal cortex (dlPFC) actuator. A local data-driven task-actuator model was identified around the cue-offset mnemonic state and used to design linear-quadratic regulation. Increasing memory load produced a strong monotonic rise in realized post-cue control effort, driven primarily by sustained dlPFC recruitment. Cue-aligned selective routing supported higher mnemonic loads with substantially less control effort than spatially nonspecific routing. Mean-matched open-loop stimulation reproduced much of the nominal retention benefit, whereas state-dependent feedback provided greater robustness when mnemonic activity was perturbed. Finite-horizon analysis revealed a strongly anisotropic, effectively low-dimensional control geometry dominated by a common mnemonic direction, with much weaker access to item-differentiating directions. These results link increasing working-memory demand to greater sustained prefrontal control requirements and show how frontoparietal routing geometry shapes the efficiency and robustness of mnemonic regulation.

neuroscience↗

bioRxiv2026

Parallel control of conjunctive and compositional representations supports dynamic task preparation

People can dynamically and adaptively update task goals in the face of task uncertainty. In this fMRI study, we aimed to investigate the modulation of neural task representations that subserve such flexible task control. On each trial, we asked people to perform one of nine image categorization tasks. During task preparation, participants had to actively infer varying levels of task uncertainty and dynamically modulate their task preparation accordingly. Multivariate pattern analyses demonstrated dissociable uncertainty-driven modulations of conjunctive and compositional task representations in the right frontoparietal network. Specifically, different sub-regions showed diminished conjunctive task representations when task uncertainty increased during task preparation. At the same time, we observed an active maintenance of compositional task representations, suggesting an adaptive cognitive strategy in facilitating compositional task reconfiguration. These findings suggest a mechanism of parallel control on conjunctive and compositional representations that allows for maximizing the advantages of both representational formats, offering new insights into the neural mechanisms underpinning human flexible task preparation.

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bioRxiv2025

Dorsomedial Prefrontal Cortex links abstract planning to motor execution

Mental planning is essential for producing action sequences. Despite the contribution of planning to many everyday activities, the neurocognitive processes that map a selected plan into a concrete course of action are unclear. We asked whether planning and execution are linked by abstract task relationships that are divorced from the specifics of action implementation. Human participants underwent functional MRI while performing a task that required encoding and maintaining abstract representations in order to plan and later apply those representations to execute action sequences. Our analyses revealed that dorsomedial prefrontal cortex encoded representations during the planning period that shifted progressively from information based on perceptual input to information associated with the abstract task context. These abstract representations were then used to translate between the action plan and its execution irrespective of the perceptual and motor details, indicating that DMPFC builds and sustains an abstract representational bridge that links planning to action.

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bioRxiv2024

Lesions of anterior cingulate cortex disrupt an electrophysiological signature of reward processing in humans

The reward positivity (RewP) is an event-related brain potential (ERP) component associated with feedback and reward processing. Although the component is said to be generated in anterior cingulate cortex (ACC), this inference is disputed because of the inverse problem. Recently, by conducting a current source density analysis of intracranial electroencephalogram (EEG) data recorded from a large cohort of epilepsy patients, we provided direct evidence that the RewP is produced by a circumscribed region in caudal ACC corresponding to Brodmann areas 24c and 32. In the present study we confirm that this brain area is the source of the RewP by examining the effects of damage to frontal cortex on RewP amplitude. We recorded scalp EEG from 68 stroke patients with damage to frontal cortex while they engaged in a trial-and-error guessing task used to elicit a canonical RewP. Application of non-parametric voxel-based lesion-symptom mapping to the lesion data revealed that damage to Brodmann areas 24c and 32 attenuated RewP amplitude, whereas damage to other parts of frontal cortex did not affect it. These results provide causal evidence that the caudal ACC generates the RewP and underscore the contribution of this brain region toward motivating extended behaviours. Significance statementThe reward positivity (RewP) is an event-related brain potential component that reflects reward processing in the brain. Although multiple studies have suggested that anterior cingulate cortex (ACC) is the neural generator of the RewP, this assertion is disputed mainly because of the inverse problem. In this study, we present direct evidence that the RewP is generated in caudal ACC by performing voxel-based lesion-symptom mapping (VLSM) in a cohort of 68 stroke patients with lesions in the frontal lobe. We found that a circumscribed region in right caudal ACC was significantly associated with a reduced RewP, providing the first causal evidence that this region generates the RewP in humans. These fundings elucidate the central role ACC plays in motivating extended behaviours.

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bioRxiv2024

Right posterior theta reflects human parahippocampal phase resetting by salient cues during goal-directed navigation

Animal and computational work indicate that phase resetting of theta oscillations (4-12 Hz) in the parahippocampal gyrus (PHG) by salient events (e.g., reward, landmarks) facilitates the encoding of goal-oriented information during navigation. Although well-studied in animals, this mechanism has not been empirically substantiated in humans. In the present article, we present data from two studies (Study 1: asynchronous EEG-MEG | Study 2: simultaneous EEG-fMRI) to investigate theta phase resetting and its relationship to PHG BOLD activation in healthy adults (aged 18-34 years old) navigating a virtual T-maze to find rewards. In the first experiment, both EEG and MEG data revealed a burst of theta power over right-posterior scalp locations following feedback onset (termed right-posterior theta, RPT), and RPT power and measures of phase resetting were sensitive to the subjects spatial trajectory. In Experiment 2, we used probabilistic tractography data from the human connectome project to segment the anterior and posterior PHG based on differential connectivity profiles to other brain regions. This analysis resulted in a PHG subdivision consisting of four distinct anterior and two posterior PHG clusters. Next, a series of linear mixed effects models based on simultaneous EEG-fMRI data revealed that single-trial RPT peak power significantly predicted single-trial hemodynamic responses in two clusters within the posterior PHG and one in the anterior PHG. This coupling between RPT power and PHG BOLD was exclusive to trials performed during maze navigation, and not during a similar task devoid of the spatial context of the maze. These findings highlight a role of PHG theta phase resetting for the purpose of encoding salient information during goal-directed spatial navigation. Taken together, RPT during virtual navigation integrates experimental, computational, and theoretical research of PHG function in animals with human cognitive electrophysiology studies and clinical research on memory-related disorders such as Alzheimers disease.

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bioRxiv2023

The successor representation subserves hierarchical abstraction for goal-directed behavior

Humans have the ability to craft abstract, temporally extended and hierarchically organized plans. For instance, when considering how to make spaghetti for dinner, we typically concern ourselves with useful "subgoals" in the task, such as cutting onions, boiling pasta, and cooking a sauce, rather than particulars such as how many cuts to make to the onion, or exactly which muscles to contract. A core question is how such decomposition of a more abstract task into logical subtasks happens in the first place. Previous research has shown that humans are sensitive to a form of higher-order statistical learning named "community structure". Community structure is a common feature of abstract tasks characterized by a logical ordering of subtasks. This structure can be captured by a model where humans learn predictions of upcoming events multiple steps into the future, discounting predictions of events further away in time. One such model is the "successor representation", which has been argued to be useful for hierarchical abstraction. As of yet, no study has convincingly shown that this hierarchical abstraction can be put to use for goal-directed behavior. Here, we investigate whether participants utilize learned community structure to craft hierarchically informed action plans for goal-directed behavior. Participants were asked to search for paintings in a virtual museum, where the paintings were grouped together in "wings" representing community structure in the museum. We find that participants choices accord with the hierarchical structure of the museum and that their response times are best predicted by a successor representation. The degree to which the response times reflect the community structure of the museum correlates with several measures of performance, including the ability to craft temporally abstract action plans. These results suggest that successor representation learning subserves hierarchical abstractions relevant for goal-directed behavior. AUTHOR SUMMARYHumans have the ability to achieve a diverse range of goals in a highly complex world. Classic theories of decision making focus on simple tasks involving single goals. In the current study, we test a recent theoretical proposal that aims to address the flexibility of human decision making. By learning to predict the upcoming events, humans can acquire a model of the world which they can then leverage to plan their behavior. However, given the complexity of the world, planning directly over all possible events can be overwhelming. We show that, by leveraging this predictive model, humans group similar events together into simpler "hierarchical" representations, which makes planning over these hierarchical representations markedly more efficient. Interestingly, humans seem to learn and remember both the complex predictive model and the simplified hierarchical model, using them for distinct purposes.

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bioRxiv2021

Task-level value affects trial-level reward processing and control

Despite disagreement about how anterior cingulate cortex (ACC) supports decision making, a recent hypothesis suggests that activity in this region is best understood in the context of a task or series of tasks. One important task-level variable is average reward because it is both a known driver of effortful behaviour and an important determiner of the tasks in which we choose to engage. Here we asked how average task value affects reward-related ACC activity. To answer this question, we measured a reward-related signal said to be generated in ACC called the reward positivity (RewP) while participants gambled in three tasks of differing average value. The RewP was reduced in the high-value task, an effect that was not explainable by either reward magnitude or outcome expectancy. This result suggests that ACC does not evaluate outcomes and cues in isolation, but in the context of the value of the current task.

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bioRxiv2021

Alpha Event-related Desynchronization During Reward Processing in Schizophrenia

BackgroundDeficits in the way the brain processes rewards may contribute to negative symptoms in schizophrenia. Synchronization of alpha band neural oscillations is a dominant EEG signal when people are awake, but at rest. In contrast, alpha desynchronization to salient events is thought to direct allocation of information processing resources away from the internal state, to process salient stimuli in the external environment. Here, we hypothesize that alpha event-related desynchronization (ERD) during reward processing is altered in schizophrenia, leading to less difference in alpha ERD magnitude between winning and losing outcomes. MethodsEEG was recorded while participants (patients with schizophrenia (SZ)=54; healthy controls (HC) = 54) completed a casino-style slot machine gambling task. Total power, a measure of neural oscillation magnitude was measured in the alpha frequency range (8-14 Hz), time-locked to reward delivery, extracted via principal components analysis, and then compared between groups and equiprobable win and near miss loss reward outcomes. Associations between alpha power and negative symptoms and trait rumination were examined. ResultsA significant Group X Reward Outcome interaction (p=.018) was explained by differences within the HC group, driven by significant posterior-occipital alpha desynchronization to wins, relative to near miss losses (p<.001). In contrast, SZ did not modulate alpha power to wins vs. near miss losses (p>.1), nor did alpha power relate to negative symptoms (p>.1). However, across all participants, less alpha ERD to reward outcomes was related to more trait rumination, for both wins (p=.005) and near-miss losses (p=.002), with no group differences observed in the slopes of these relationships. ConclusionThese findings suggest that event-related modulation of alpha power is altered in schizophrenia during reward outcome processing, even when reward attainment places minimal demands on higher-order cognitive processes during slot machine play. In addition, high trait rumination is associated with less event-related desynchronization to reward feedback, suggesting that rumination covaries with less external attentional allocation to reward processing, regardless of reward outcome valence and group membership.

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bioRxiv2020

Reward processing electrophysiology in schizophrenia: Effects of age and illness phase

BackgroundReward processing abnormalities may underlie characteristic pleasure and motivational impairments in schizophrenia. Some neural measures of reward processing show strong age-related modulation, highlighting the importance of considering age effects on reward sensitivity. We compared event-related potentials (ERPs) reflecting reward anticipation (stimulus-preceding negativity, SPN) and evaluation (reward positivity, RewP; late-positive potential, LPP) across individuals with schizophrenia (SZ) and healthy controls (HC), with an emphasis on examining effects of chronological age, brain age (i.e., predicted age based on neurobiological measures), and illness phase. MethodsSubjects underwent EEG while completing a slot-machine task for which rewards were not dependent on performance accuracy, speed, or other preparatory demands. Slot-machine task EEG responses were compared between 54 SZ and 54 HC individuals, ages 19 to 65. Reward-related ERPs were analyzed with respect to chronological age, categorically-defined illness phase (early; ESZ versus chronic schizophrenia; CSZ), and were used to model brain age relative to chronological age. ResultsIllness phase-focused analyses indicated there were no group differences in average SPN or RewP amplitudes. However, a group x reward outcome interaction revealed that ESZ differed from HC in later outcome processing, reflected by greater LPP responses following loss versus reward (a reversal of the HC pattern). While brain age estimates did not differ among groups, depressive symptoms in SZ were associated with older brain age estimates while controlling for negative symptoms. ConclusionsESZ and CSZ did not differ from HC in reward anticipation or early outcome processing during a cognitively undemanding reward task, highlighting areas of preserved functioning. However, ESZ showed altered later reward outcome evaluation, pointing to selective reward deficits during the early illness phase of schizophrenia. Further, an association between ERP-derived brain age and depressive symptoms in SZ extends prior findings linking depression with reward-related ERP blunting. Taken together, both illness phase and age may impact reward processing in SZ, and brain aging may offer a promising, novel marker of reward dysfunction that warrants further study.

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bioRxiv2019

Electrophysiological correlates of state transition prediction errors

Planning behavior depends crucially on the ability to distinguish between the likely and unlikely consequences of an action. Formal computational models of planning postulate the existence of a neural mechanism that tracks the transition model of the environment, i.e., a model that explicitly represents the probabilities of action consequences. However, empirical findings relating to such a mechanism are scarce. Here we report the results of two electroencephalographic experiments examining the neural correlates of transition model learning. The results implicate fronto-midline theta and delta oscillations in this process and suggest a role of the anterior midcingulate cortex in planning behavior.

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bioRxiv2018

Subgoal- and Goal-Related Prediction Errors in Medial Prefrontal Cortex

A longstanding view of the organization of human and animal behavior holds that behavior is hierarchically organized, meaning that it can be understood as directed towards achieving superordinate goals through subordinate goals, or subgoals. For example, the superordinate goal of making coffee can be broken down as accomplishing a series of subgoals, namely boiling water, grinding coffee, pouring cream, etc. Learning and behavioral adaptation depend on prediction-error signals, which have been observed in ventral striatum (VS) and medial prefrontal cortex (mPFC). In past work, we have shown that prediction error signals (PEs) can be linked not only to superordinate goals, but also to subgoals. Here we present two functional magnetic resonance imagining experiments that replicate and extend these findings. In the first experiment, we replicated the finding that mPFC signals subgoal-related PEs, independently of goal PEs. Together with our past work, this experiment reveals that BOLD responses to PEs in mPFC are unsigned. In the second experiment, we showed that when a task involves both goal and subgoal PEs, mPFC shows only goal-related PEs, suggesting that context or attention can strongly impact hierarchical PE coding. Furthermore, we observed a dissociation between the coding of PEs in mPFC and VS. These experiments suggest that the mPFC selectively attends to information at different levels of hierarchy depending on the task context.

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bioRxiv2017

Electrophysiological indices of anterior cingulate cortex function reveal changing levels of cognitive effort and reward valuation that sustain task performance

Successful execution of goal-directed behaviors often requires the deployment of cognitive control, which is thought to require cognitive effort. Recent theories have proposed that anterior cingulate cortex (ACC) regulates control levels by weighing the reward-related benefits of control against its effort-related costs. However, given that the sensations of cognitive effort and reward valuation are available only to introspection, this hypothesis is difficult to investigate empirically. We have proposed that two electrophysiological indices of ACC function, frontal midline theta and the reward positivity (RewP), provide objective measures of these functions. To investigate this issue, we recorded the electroencephalogram (EEG) from participants engaged in an extended, cognitively-demanding task. Participants performed a time estimation task for 2 hours in which they received reward and error feedback according to their task performance. We observed that the amplitude of the RewP, a feedback-locked component of the event related brain potential associated with reward processing, decreased with time-on-task. Conversely, frontal midline theta power, which consists of 4-8 Hz EEG oscillations associated with cognitive effort, increased with time-on-task. We also examined how these phenomena changed over time by conducting within-participant multi-level modeling analyses. Our results suggest that extended execution of a cognitively-demanding task is characterized by an early phase in which high control levels combine with strong reward valuation to foster rapid improvements in task performance, and a later phase in which high control levels counteract waning reward valuation to maintain stable task performance.

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bioRxiv2017

Episodic, Semantic, Pavlovian, and Procedural Cognitive Maps

Current theories of planning associate the hippocampus with a cognitive map, a theoretical construct used to predict the consequences of actions. This formulation is problematic for two reasons: First, cognitive maps are traditionally conceptualized to generalize over individual episodes, which conflicts with evidence associating the hippocampus with episodic memory, and second, it fails to explain seemingly non-hippocampal forms of planning. Here we propose a novel theoretical framework that resolves these issues: each long-term memory system is a cognitive map, predicting consequences of actions based on its unique computational properties. It follows that hippocampal maps are episode-based and that semantic, procedural, and Pavlovian memories each implement a specialized map. We present evidence for each type of map from neuropsychology, neuroimaging and animal electrophysiology studies.

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