Biology subjects

Buckley, M. J.

Publications and source records attributed to Buckley, M. J..

11 recordsLinked to original sources

bioRxiv2026

Attentional selection drives information convergence within macaque lateral prefrontal cortex

Attention is a coherent state, in which multiple brain regions converge to represent selected features of a focal object or event. Lateral prefrontal cortex (LPFC), with its flexible coding of multiple task features and their conjunctions, is widely believed to play a key role in this process. While much research has investigated biased competition between features within a brain region, and cofluctuations of activity between regions, less is known about the representational dynamics through which a coherent neural state emerges. Here, we examine directed mutual information concerning multiple feature-specific population codes, between dorsal and ventral LPFC, across three phases of an attentional selection task. We find bidirectional convergence of information regarding multiple task features, but specifically following the period of selection from the visual display. The results show that neural processes driving inter-region coherence are especially salient during a period of cued object selection, despite comparable local information representation during other task phases. Significance statementIn the primate brain, lateral prefrontal cortex (LPFC) is thought to play a key role in selective attention, which is fundamental to goal-directed behaviour, and implies inter-region convergence towards a coherent representational state. Combining neural recordings, multivariate decoding, and analysis of information dynamics, we find local representations of multiple task features during multiple task phases, in separate regions of LPFC, with strong inter-region representational coherence emerging when attention could be directed to a chosen target. Results show that information convergence between these regions is bidirectional, sustained, and reflects multiple features of a chosen object, but, unlike local information representation, is highly specific to the choice phase of the task.

neuroscience↗

bioRxiv2025

Neural dynamics of an extended frontal lobe network in goal-subgoal problem solving

In goal-directed behavior, cognitive control calls for representation of current state, goal state, and current move, often with hierarchical organization into a series of steps or subgoals. In the human brain, a network of multiple-demand or MD regions underpins cognitive control, and core task features are likely encoded and integrated across this distributed network. Here we recorded from four putative homologs to human MD regions in the frontal cortex -- ventrolateral (vlPFC), dorsomedial (dmPFC), dorsal premotor (dPM) and anterior insula/orbitofrontal (I/O) cortex -- as two male monkeys solved a multi-step, on-screen spatial maze. Across regions there was substantial overlap but also wide quantitative variation in encoding task variables. Sensory input and current state were strongly coded in vlPFC, goal most stably in dmPFC, and move most rapidly in vlPFC and dPM. I/O responded during revision of a prepared route. In all regions, an abstract code of problem structure marked progress from problem start to end, with hierarchical separation of progress within and between successive steps. Partial specialisations, we suggest, arise from distinct connectivity, while broad co-recruitment reflects strong information exchange. Our results show how core components of goal-directed behavior are encoded across a distributed network of partial frontal lobe specialists, putatively homologous to frontal components of the human MD system.

neuroscience↗

bioRxiv2024

Frontopolar cortex stimulation induces prolonged disruption to counterfactual processing: insights from altered local field potentials

Frontopolar cortex (FPC) is a large, anterior sub-region of prefrontal cortex found in both humans and non-human primates (NHPs) and is thought to support monitoring the value of switching between alternative goals. However, the neuronal mechanisms underlying this function are unclear. Here we used multielectrode arrays to record the local field potentials (LFPs) in the FPC of two macaques performing a Wisconsin Card Sorting Test analogue and found that bursts of gamma and beta in FPC tracked counterfactual not current rule value. Moreover, we show that brief high-frequency microstimulation to a single trial causally affects both LFP activity in FPC, as well as rule-guided decision-making across successive trials. Following stimulation of FPC we observed reduced exploration of the counterfactual rule pre-rule-change, as well as a delayed adaptation to the newly relevant following post-rule-change. A similar, multi-trial time-course disturbance to beta and gamma activity within FPC was also induced following single-trial microstimulation. These findings conclusively link neuronal activity in FPC with behavioural monitoring of the value of counterfactual rules and provide neural mechanistic insights into how FPC supports rule-based decision-making. Significance statementIncreasing evidence from human and non-human primates has prompted theories linking FPC with the control of exploration during decision-making. However, it is current unclear how the neuronal activity within frontal pole supports exploratory decision-making processes. Here we show that rhythmic activity, in the beta and gamma bands, recorded from FPC is correlated both with outcome of the previous choice, and the value of switching to an alternative choice. Furthermore, we show that disrupting beta and gamma activity within FPC causally influences exploratory decision-making: initially decreasing exploration before impairing adaptation to abstract rule changes. Together these findings provide the first mechanistic insight into how the neuronal activity within FPC can support exploratory behaviour.

neuroscience↗

bioRxiv2022

Tracking subject's strategies in behavioural choice experiments at trial resolution

Investigating how, when, and what subjects learn during decision-making tasks requires tracking their choice strategies on a trial-by-trial basis. Here we present a simple but effective probabilistic approach to tracking choice strategies at trial resolution using Bayesian evidence accumulation. We show this approach identifies both successful learning and the exploratory strategies used in decision tasks performed by humans, non-human primates, rats, and synthetic agents. Both when subjects learn and when rules change the exploratory strategies of win-stay and lose-shift, often considered complementary, are consistently used independently. Indeed, we find the use of lose-shift is strong evidence that subjects have latently learnt the salient features of a new rewarded rule. Our approach can be extended to any discrete choice strategy, and its low computational cost is ideally suited for real-time analysis and closed-loop control.

neuroscience↗

bioRxiv2020

A one-shot learning signal in monkey prefrontal cortex

Much animal learning is slow, with cumulative changes in behavior driven by reward prediction errors. When the abstract structure of a problem is known, however, both animals and formal learning models can rapidly attach new items to their roles within this structure, sometimes in a single trial. Frontal cortex is likely to play a key role in this process. To examine information seeking and use in a known problem structure, we trained monkeys in a novel explore/exploit task, requiring the animal first to test objects for their association with reward, then, once rewarded objects were found, to re-select them on further trials for further rewards. Many cells in the frontal cortex showed an explore/exploit preference, changing activity in a signal trial to align with one-shot learning in the monkeys behaviour. In contrast to this binary switch, these cells showed little evidence of continuous changes linked to expectancy or prediction error. Explore/exploit preferences were independent for two stages of the trial, object selection and receipt of feedback. Within an established task structure, frontal activity may control the separate operations of explore and exploit, switching in one trial between the two. Significance statementMuch animal learning is slow, with cumulative changes in behavior driven by reward prediction errors. When the abstract structure a problem is known, however, both animals and formal learning models can rapidly attach new items to their roles within this structure. To address transitions in neural activity during one-shot learning, we trained monkeys in an explore/exploit task using familiar objects and a highly familiar task structure. In contrast to continuous changes reflecting expectancy or prediction error, frontal neurons showed a binary, one-shot switch between explore and exploit. Within an established task structure, frontal activity may control the separate operations of exploring alternative objects to establish their current role, then exploiting this knowledge for further reward.

neuroscience↗

bioRxiv2020

Prefrontal neural dynamics for behavioral decisions and attentional control

Complex neural dynamics in the prefrontal cortex contribute to context-dependent decisions and attentional competition. To analyze these dynamics, we apply demixed principal component analysis to activity of a primate prefrontal cell sample recorded in a cued target detection task. The results track dynamics of cue and object coding, feeding into movements along a target present-absent decision axis in a low-dimensional subspace of population activity. For a single stimulus, object and cue coding are seen mainly in the contralateral hemisphere. Later, a developing decision code in both hemispheres may reflect interhemispheric communication. With a target in one hemifield and a competing nontarget in the other, each hemisphere initially encodes the contralateral object, but finally, decision coding is dominated by the task-relevant target. These findings further suggest that exchange of information between hemispheres plays a key role when attentional competition resolves. Tracking complex neural events in a low-dimensional activity subspace illuminates integration of neural codes towards task-appropriate behavior, comprising a building block of learned task structure in the prefrontal cortex. AUTHOR SUMMARYFlexible adaptive processing of information is integral for everyday goal-directed behavior. To unravel dynamic representation of task-relevant information, we analyzed population activity of a primate prefrontal cell sample in a cued target detection task. In a low-dimensional neural subspace, with separate axes for cue, object identity and decision, trajectories showed initial coding of cue and object in the contralateral hemisphere, followed by coding of the behavioral decision across both hemispheres. With target and nontarget stimuli in opposite hemifields, the data suggest initial coding of the contralateral object in each hemisphere. Object coding is then rapidly shut off for the nontarget, and followed by bilateral coding of the target decision. The results bring detailed insight into task structure and information flow within and between the two frontal lobes as a decision is made and attentional competition is resolved.

neuroscience↗

bioRxiv2020

Double-dissociation of frequency-specific contributions of dorso-lateral and dorso-medial prefrontal cortex to familiarity and recollective processes in the primate

According to dual-process theories, recognition memory draws upon both familiarity and recollection. It remains unclear how primate prefrontal cortex (PFC) contributes to familiarity and recollection processes but frequency-specific neuronal activities are considered to play a key role. Here, non-human primate (NHP) electrophysiological local field potential (LFP) recordings first showed that a specific subregion of macaque PFC (i.e., dorsolateral PFC, dlPFC) was implicated in task performance at a specific frequency (i.e., increased beta power in the 10-15 Hz range observed in correct versus error trials) in a specific phase of a recognition memory task (i.e., during sample presentation). Then, to assess generalization to humans and causality we targeted left human dlPFC (BA 9/46) as well as left dorsomedial prefrontal cortex (BA 8/9) for comparison, and also vertex as a control, with transcranial magnetic stimulation at a frequency in the middle of the low-beta range observed in NHP (i.e. 12.5 Hz) and compared that to non-frequency-specific stimulation, and also to a no-stimulation control, during occasional sample presentations within a similar task. Hence we investigated hypotheses about the causal importance for human memory of a location-specific, frequency-specific, and task-epoch-specific intervention derived directly from the NHP electrophysiological observations. Using a dual-process signal detection (DPSD) model based on analysing receiver operating characteristics (ROC) curves, we showed beta-frequency TMS caused decreased recollection when targeted to human dlPFC, but enhanced familiarity when targeted to dorsomedial prefrontal cortex. Non-frequency-specific patterns of stimulation to all sites, and beta-frequency stimulation to vertex, were all without behavioural effect. This study provides causal evidence that PFC-mediated contributions to object recognition memory are modulated by beta-frequency activity; more broadly it provides translational evidence bridging NHPs and humans by emphasizing functional roles of beta-frequency activity in homologous brain regions in recognition memory. HighlightsO_LIlow beta power in NHP dlPFC during stimulus encoding was related to behaviour C_LIO_LIhuman rTMS study used parameters derived from NHP observations to test causality C_LIO_LIlow beta rTMS to human dlPFC, but not dmPFC, impairs recollection C_LIO_LIlow beta rTMS to human dmPFC, but not dlPFC, enhances familiarity C_LIO_LIprovides cross-species validation of prefrontal beta power to primate recognition C_LI

neuroscience↗

bioRxiv2020

Similar time course of fast familiarity and slow recollection processes for recognition memory in humans and macaques

According to dual-process theory, recognition memory performance draws upon two processes, familiarity and recollection. The relative contribution to recognition memory are commonly distinguished in humans by analyzing receiver-operating-characteristics (ROC) curves; analogous methods are more complex and very rare in animals but fast familiarity and slow recollective-like processes (FF/SR) have been detected in non-human primates (NHPs) based on analyzing recognition error response time profiles. The relative utility of these methods to investigate familiarity and recollection/recollection-like processes across species is uncertain; indeed, even how comparable the FF/SR measures are across humans and NHPs remains unclear. Therefore in this study a broadly similar recognition memory task was exploited in both humans and NHPs to investigate the time course of the two recognition processes. We first show that the FF/SR dissociation exists in this task in human participants and then we demonstrate a similar profile in NHPs which suggests that FF/SR processes are comparable across species. We then verified, using ROC-derived indices for each time-bin in the FF/SR profile, that the ROC and FF/DR measures are related. Hence we argue that the FF/SR approach, procedurally easier in animals, can be used as a decent proxy to investigate these two recognition processes in future animal studies, important given that scant data exists as to the neural basis underlying recollection yet many of the most informative techniques primarily exist in animal models.

animal behavior and cognition↗

bioRxiv2019

Frontopolar cortex is a mediator of network modularity in the primate brain

Primate frontopolar cortex (FPC), occupied by area 10, sits atop a functional hierarchy of prefrontal cortical regions yet little is known about its causal role influencing cognition and brain networks. We studied resting-state-functional-connectivity (rsfc) networks in rhesus monkeys with or without FPC; 86 cortical regions showed significant differences in inter-area rsfc measures in lesioned animals versus controls. K-means clustering showed these regions were organized into two distinct networks in lesioned animals, whereas the same areas clustered into four networks in control animals. These networks extended within and beyond prefrontal cortex. These results suggest that FPC is involved in mediating cortical networks in the primate brain, both within and beyond prefrontal cortex. Even after 40 months only partial recovery of lesion-induced reduced modularity had occurred. We therefore suggest that FPC might help implement long-standing diverse neural network dynamics.

neuroscience↗

bioRxiv2018

Mnemonic introspection in macaques is dependent on dorsolateral prefrontal but not orbitofrontal cortex

The human prefrontal cortex (PFC) has been associated more with meta-perceptual as opposed to meta-memory decisions from correlational neuroimaging investigations. Recently, metacognitive abilities have also been shown to be causally dependent upon anterior and dorsal PFC in non-human primate lesion studies. Two studies, utilizing post-decision wagering paradigms and reversible inactivation, challenged this meta-perceptual versus meta-memory notion and showed that dorsal and anterior prefrontal areas are associated with metamemory for experienced objects and awareness of ignorance respectively. Causal investigations are important but scarce; nothing is known, for example, about the causal contributions of prefrontal sub-regions to spatial metamemory. Here, we investigated the effects of dorsal versus ventral PFC lesions on two-alternative forced choice spatial discrimination tasks in male macaque monkeys. Importantly, we were rigorous in approach and applied three independent but complementary indices used to quantify individual animals metacognitive ability ("type II sensitivity") namely meta-d', d' measures, and Phi coefficient ({Phi}). Our results were consistent across indices: while neither lesions to superior dorsolateral PFC (sdlPFC) nor orbitofrontal cortex (OFC) impaired spatial recognition performance, only monkeys with sdlPFC lesions were impaired in meta-accuracy. Together with the observation that the same OFC lesioned monkeys were impaired in updating rule-value in a Wisconsin Card Sorting Test analog, we therefore document a functional double-dissociation between these two PFC regions. Out study presents important causal evidence that other dimensions, namely domain-specific processing (e.g., spatial versus non-spatial metamemory), also need considerations in understanding the functional specialization in the neural underpinnings of introspection. Significance StatementThis study demonstrates macaque monkeys meta-cognitive capability of introspecting its own memory success is causally dependent on intact superior dorsolateral prefrontal cortices (PFC) but not the orbitofrontal cortices. Combining neurosurgical techniques on monkeys and state-of-the-art measures of metacognition, we affirm a critical role of the PFC in supporting spatial meta-recognition memory and delineate functional specificity within PFC for distinct elements of metacognition.

neuroscience↗

bioRxiv2017

Functional reorganisation and recovery following cortical lesions: A study in macaque monkeys

Damage following traumatic brain injury or stroke can often extend beyond the boundaries of the initial insult and can lead to maladaptive cortical reorganisation. On the other hand, beneficial cortical reorganisation leading to recovery of function can also occur. Here, we used resting state FMRI (rsFMRI) to examine how functional connectivity in the macaque brain changed across time in response to lesions to the prefrontal cortex, and how this reorganisation correlated with changes in behaviour. Two monkeys were trained to perform location-based and object-based delayed match-to-sample tasks. We also collected rsFMRI data under general anaesthesia at two pre-lesion time-points, separated by 3-4 weeks. After two cycles of testing and scanning, the animals received a principal sulcus lesion followed by an additional 4 cycles of testing and scanning. Later, the same animals received a second lesion to the opposite hemisphere and additional cycles of testing and scanning.\n\nBoth animals showed a marked behavioural impairment following the first lesion, which was associated with a decrease in functional connectivity, predominantly within frontal-frontal networks in both hemispheres. Approximately 8 weeks following the lesion, performance improved, as did functional connectivity within these networks. Following the second lesion, functional connectivity again decreased and this was associated with a marginal behavioural deficit that did not recover.\n\nOur data show that behavioural impairments reflect not just the removal of the lesioned area, but also disturbance to an extensive cortical network. This network can recover by restoring and/or strengthening pre-existing connections, leading to improvement in behaviour.

neuroscience↗