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Friston, K. J.

Publications and source records attributed to Friston, K. J..

10 recordsLinked to original sources

Hippocampal-entorhinal transformations in abstract frames of reference

Knowing how anothers preferences relate to our own is a central aspect of everyday decision-making, yet how the brain performs this transformation is unclear. Here, we ask whether the putative role of the hippocampal-entorhinal system in transforming relative and absolute spatial coordinates during navigation extends to transformations in abstract decision spaces. During fMRI scanning, subjects learned a strangers preference for an everyday activity - relative to one of three personally known individuals - and subsequently decided how the strangers preference relates to the other two individuals preferences. We found that entorhinal cortex/subiculum signals exhibited reference frame-sensitive responses to the absolute distance between the ratings of the stranger and the familiar choice options. In contrast, striatal signals increased when accurately determining the ordinal position of choice options in relation to the stranger. Paralleling its role in navigation, these data implicate the entorhinal/subicular region in assimilating relatively coded knowledge within abstract metric spaces.

neuroscience

Computational mechanisms of curiosity and goal-directed exploration

Successful behaviour depends on the right balance between maximising reward and soliciting information about the world. Here, we show how different types of information-gain emerge when casting behaviour as surprise minimisation. We present two distinct mechanisms for goal-directed exploration that express separable profiles of active sampling to reduce uncertainty. Hidden state exploration motivates agents to sample unambiguous observations to accurately infer the (hidden) state of the world. Conversely, model parameter exploration, compels agents to sample outcomes associated with high uncertainty, if they are informative for their representation of the task structure. We illustrate the emergence of these types of information-gain, termed active inference and active learning, and show how these forms of exploration induce distinct patterns of Bayes-optimal behaviour. Our findings provide a computational framework to understand how distinct levels of uncertainty induce different modes of information-gain in decision-making.

neuroscience

Human hippocampal theta oscillations reflect sequential dependencies during spatial planning.

Movement-related theta oscillations in rodent hippocampus coordinate forward sweeps of location-specific neural activity that could be used to evaluate spatial trajectories online. This raises the possibility that increases in human hippocampal theta power accompany the evaluation of upcoming spatial choices. To test this hypothesis, we measured neural oscillations during a spatial planning task that closely resembles a perceptual decision-making paradigm. In this task, participants searched visually for the shortest path between a start and goal location in novel mazes that contained multiple choice points, and were subsequently asked to make a spatial decision at one of those choice points. We observed ~4-8 Hz hippocampal/medial temporal lobe theta power increases specific to sequential planning that were negatively correlated with subsequent decision speed, where decision speed was inversely correlated with choice accuracy. These results implicate the hippocampal theta rhythm in decision tree search during planning in novel environments.

neuroscience

Locus Coeruleus tracking of prediction errors optimises cognitive flexibility: an Active Inference model.

The locus coeruleus (LC) in the pons is the major source of noradrenaline (NA) in the brain. Two modes of LC firing have been associated with distinct cognitive states: changes in tonic rates of firing are correlated with global levels of arousal and behavioural flexibility, whilst phasic LC responses are evoked by salient stimuli. Here, we unify these two modes of firing by modelling the response of the LC as a correlate of a prediction error when inferring states for action planning under Active Inference (AI).\n\nWe simulate a classic Go/No-go reward learning task and a three-arm foraging task and show that, if LC activity is considered to reflect the magnitude of high level state-action prediction errors, then both tonic and phasic modes of firing are emergent features of belief updating. We also demonstrate that when contingencies change, AI agents can update their internal models more quickly by feeding back this state-action prediction error - reflected in LC firing and noradrenaline release - to optimise learning rate, enabling large adjustments over short timescales. We propose that such prediction errors are mediated by cortico-LC connections, whilst ascending input from LC to cortex modulates belief updating in anterior cingulate cortex (ACC).\n\nIn short, we characterise the LC/ NA system within a general theory of brain function. In doing so, we show that contrasting, behaviour-dependent firing patterns are an emergent property of the LCs crucial role in translating prediction errors into an optimal mediation between plasticity and stability.\n\nAuthor SummaryThe brain uses sensory information to build internal models and make predictions about the world. When errors of prediction occur, models must be updated to ensure desired outcomes are still achieved. Neuromodulator chemicals provide a possible pathway for triggering such changes in brain state. One such neuromodulator, noradrenaline, originates predominantly from a cluster of neurons in the brainstem - the locus coeruleus (LC) - and plays a key role in behaviour, for instance, in determining the balance between exploiting or exploring the environment.\n\nHere we use Active Inference (AI), a mathematical model of perception and action, to formally describe LC function. We propose that LC activity is triggered by errors in prediction and that the subsequent release of noradrenaline alters the rate of learning about the environment. Biologically, this describes an LC-cortex feedback loop promoting behavioural flexibility in times of uncertainty. We model LC output as a simulated animal performs two tasks known to elicit archetypal responses. We find that experimentally observed phasic and tonic patterns of LC activity emerge naturally, and that modulation of learning rates improves task performance. This provides a simple, unified computational account of noradrenergic computational function within a general model of behaviour.

neuroscience

Generalised free energy and active inference: can the future cause the past?

We compare two free energy functionals for active inference under Markov decision processes. One of these is a functional of beliefs about states and policies, but a function of observations, while the second is a functional of beliefs about all three. In the former (expected free energy), prior beliefs about outcomes are not part of the generative model (because they are absorbed into the prior over policies). Conversely, in the second (generalised free energy); priors over outcomes become an explicit component of the generative model. When using the free energy function, which is blind to counterfactual (i.e., future) observations, we equip the generative model with a prior over policies that ensure preferred (i.e., priors over) outcomes are realised. In other words, selected policies minimise uncertainty about future outcomes by minimising the free energy expected in the future. When using the free energy functional - that effectively treats counterfactual observations as hidden states - we show that policies are inferred or selected that realise prior preferences by minimising the free energy of future expectations. Interestingly, the form of posterior beliefs about policies (and associated belief updating) turns out to be identical under both formulations, but the quantities used to compute them are not.

neuroscience

Dynamic causal modelling of fluctuating connectivity in resting-state EEG

Functional and effective connectivity are known to change systematically over time. These changes might be explained by several factors, including intrinsic fluctuations in activity-dependent neuronal coupling and contextual factors, like experimental condition and time. Furthermore, contextual effects may be subject-specific or conserved over subjects. To characterize fluctuations in effective connectivity, we used dynamic causal modelling (DCM) of cross spectral responses over 1 min of electroencephalogram (EEG) recordings during rest, divided into 1-sec windows. We focused on two intrinsic networks: the default mode and the saliency network. DCM was applied to estimate connectivity in each time-window for both networks. Fluctuations in DCM connectivity parameters were assessed using hierarchical parametric empirical Bayes (PEB). Within-subject, between-window effects were modelled with a second-level linear model with temporal basis functions as regressors. This procedure was conducted for every subject separately. Bayesian model reduction was then used to assess which (combination of) temporal basis functions best explain dynamic connectivity over windows. A third (between-subject) level model was used to infer which dynamic connectivity parameters are conserved over subjects. Our results indicate that connectivity fluctuations in the saliency network comprised both subject-specific components and a common component. For the default mode network, connectivity trajectories only showed a common component. For both networks, connections to higher order regions appear to monotonically increase during the one minute period. These results not only establish the predictive validity of dynamic connectivity estimates - in virtue of detecting systematic changes over subjects - they also suggest a network-specific dissociation in the relative contribution of fluctuations in connectivity that depend upon experimental context. We envisage these procedures could be useful for characterizing brain state transitions that may be explained by their cognitive or neuropathological underpinnings.

neuroscience

Variability and reliability of effective connectivity within the core default mode network: A longitudinal spectral DCM study

Dynamic causal modelling (DCM) for resting state fMRI - namely spectral DCM - is a recently developed and widely adopted method for inferring effective connectivity in intrinsic brain networks. Most research applying spectral DCM has focused on group-averaged connectivity within large-scale intrinsic brain networks; however, the consistency of subject- and session-specific estimates of effective connectivity has not been evaluated. Establishing reliability (within subjects) is crucial for its clinical use; e.g., as a neurophysiological phenotype of disease progression. Effective connectivity during rest is likely to vary due to changes in cognitive, behavioural, and physical states. Determining the sources of fluctuations in effective connectivity may yield greater understanding of brain processes and inform clinical applications about potential confounds. In the present study, we investigated the consistency of effective connectivity within and between subjects, as well as potential sources of variability (e.g., hemispheric asymmetry). We further investigated how standard procedures for data processing and signal extraction affect this consistency. DCM analyses were applied to four longitudinal resting state fMRI datasets. Our sample consisted of 20 subjects with 653 resting state fMRI sessions in total. These data allowed to quantify the robustness of connectivity estimates for each subject, and to draw conclusions beyond specific data features. We found that subjects contributing to all datasets showed systematic and reliable patterns of hemispheric asymmetry. When asymmetry was taken into account, subjects showed very similar connectivity patterns. We also found that various processing procedures (e.g. global signal regression and ROI size) had little effect on inference and reliability of connectivity for the majority of subjects. Bayesian model reduction increased reliability (within-subjects) and stability (between-subjects) of connectivity patterns.

neuroscience

The Perceptual Shaping of Anticipatory Actions

Humans display anticipatory motor responses to minimize the adverse effects of predictable perturbations. A widely accepted explanation for this behavior relies on the notion of an inverse model that, learning from motor errors, anticipates corrective responses. Here, we propose and validate the alternative hypothesis that anticipatory control can be realized through a cascade of purely sensory predictions that drive the motor system, reflecting the causal sequence of the perceptual events preceding the error. We compare both hypotheses in a simulated anticipatory postural adjustment task. We observe that adaptation in the sensory domain, but not in the motor one, supports the robust and generalizable anticipatory control characteristic of biological systems. Our proposal unites the neurobiology of the cerebellum with the theory of active inference and provides a concrete implementation of its core tenets with great relevance both to our understanding of biological control systems and, possibly, to their emulation in complex artefacts.

neuroscience

NMDA-receptor antibodies alter cortical microcircuit dynamics

NMDA-receptor antibodies (NMDAR-Ab) cause an autoimmune encephalitis with a diverse range of electroencephalographic (EEG) abnormalities. NMDAR-Ab are believed to disrupt receptor function, but how blocking this excitatory neurotransmitter can lead to paroxysmal EEG abnormalities - or even seizures - is poorly understood. Here, we show that NMDAR-Ab change intrinsic cortical connections and neuronal population dynamics to alter the spectral composition of spontaneous EEG activity, and predispose to paroxysmal EEG abnormalities. Based on local field potential recordings in a mouse model, we first validate a dynamic causal model of NMDAR-Ab effects on cortical microcircuitry. Using this model, we then identify the key synaptic parameters that best explain EEG paroxysms in paediatric patients with NMDAR-Ab encephalitis. Finally, we use the mouse model to show that NMDAR-Ab- related changes render microcircuitry critically susceptible to overt EEG paroxysms, when these key parameters are changed. These findings offer mechanistic insights into circuit-level dysfunction induced by NMDAR-Ab.

neuroscience

NMDA receptor blockade causes selective prefrontal disinhibition in a roving auditory oddball paradigm

N-methyl-D-aspartate receptors (NMDARs) are expressed widely throughout the human cortex. Yet disturbances in NMDAR transmission - as implicated in patients with schizophrenia or pharmacologically induced - can cause a regionally specific set of electrophysiological effects. Here, we present a double-blind placebo-controlled study of the effects of the NMDAR blocker ketamine in human volunteers. We employ a marker of auditory learning and putative synaptic plasticity - the mismatch negativity - in a roving auditory oddball paradigm. Using recent advances in Bayesian modelling of group effects in dynamic causal modelling, we fit biophysically plausible network models of the auditory processing hierarchy to whole-scalp evoked response potential recordings. This allowed us to identify the regionally specific effects of ketamine in a distributed network of interacting cortical sources. Under placebo, our analysis replicated previous findings regarding the effects of stimulus repetition and deviance on connectivity within the auditory hierarchy. Crucially, we show that the effect of ketamine is best explained as a selective change in intrinsic inhibition, with a pronounced ketamine-induced reduction of inhibitory interneuron connectivity in frontal sources. These results are consistent with findings from invasive recordings in animal models exposed to NMDAR blockers, and provide evidence that inhibitory-interneuron specific NMDAR dysfunction may be sufficient to explain electrophysiological abnormalities of sensory learning induced by ketamine in human subjects.\n\nO_TEXTBOXSignificance StatementDysfunction of N-methyl-D-aspartate receptors (NMDARs) has been implicated in a range of psychopathologies, yet mechanisms translating receptor-level abnormalities to whole-brain pathology remain unclear. We use computational modelling to infer microcircuit mechanisms by which ketamine, an NMDAR-blocker, alters brain responses to changing sequences of sounds that rely on sensory learning. This dynamic causal modelling (DCM) approach shows that ketamine-effects can be explained with brain region specific changes in inhibitory interneuron coupling alone, with a striking reduction in inhibition in the prefrontal cortex. This suggests that NMDAR-effects on excitation-inhibition balance differ between brain regions, and provides evidence from healthy human subjects that NMDAR blockade may cause prefrontal cortex disinhibition, one of the mechanisms hypothesised to underlie psychopathology in schizophrenia.\n\nC_TEXTBOX

neuroscience