Publications

The functional architectures of addition and subtraction: Network discovery using fMRI and DCM

Abstract The neuronal mechanisms underlying arithmetic calculations are not well understood but the differences between mental addition and subtraction could be particularly revealing. Using fMRI and dynamic causal modeling (DCM), this study aimed to identify the distinct neuronal architectures engaged by the cognitive processes of simple addition and subtraction. Our results revealed significantly greater activation during subtraction in regions along the dorsal pathway, including the left inferior frontal gyrus (IFG), middle portion of dorsolateral prefrontal cortex (mDLPFC), and supplementary motor area (SMA), compared with addition. Subsequent analysis of the underlying changes in connectivity – with DCM – revealed a common circuit processing basic (numeric) attributes and the retrieval of arithmetic facts. However, DCM showed that addition was more likely to engage (numeric) retrieval‐based circuits in the left hemisphere, while subtraction tended to draw on (magnitude) processing in bilateral parietal cortex, especially the right intraparietal sulcus (IPS). Our findings endorse previous hypotheses about the differences in strategic implementation, dominant hemisphere, and the neuronal circuits underlying addition and subtraction. Moreover, for simple arithmetic, our connectivity results suggest that subtraction calls on more complex processing than addition: auxiliary phonological, visual, and motor processes, for representing numbers, were engaged by subtraction, relative to addition. Hum Brain Mapp 38:3210–3225, 2017 . © 2017 Wiley Periodicals, Inc.

Experimental validation of the free-energy principle with in vitro neural networks

Abstract Empirical applications of the free-energy principle are not straightforward because they entail a commitment to a particular process theory, especially at the cellular and synaptic levels. Using a recently established reverse engineering technique, we confirm the quantitative predictions of the free-energy principle using in vitro networks of rat cortical neurons that perform causal inference. Upon receiving electrical stimuli—generated by mixing two hidden sources—neurons self-organised to selectively encode the two sources. Pharmacological up- and downregulation of network excitability disrupted the ensuing inference, consistent with changes in prior beliefs about hidden sources. As predicted, changes in effective synaptic connectivity reduced variational free energy, where the connection strengths encoded parameters of the generative model. In short, we show that variational free energy minimisation can quantitatively predict the self-organisation of neuronal networks, in terms of their responses and plasticity. These results demonstrate the applicability of the free-energy principle to in vitro neural networks and establish its predictive validity in this setting.

Computational modelling of EEG and fMRI paradigms reveals a consistent loss of pyramidal cell synaptic gain in schizophrenia

Abstract Diminished synaptic gain – the sensitivity of postsynaptic responses to neural inputs – may be a fundamental synaptic pathology in schizophrenia. Evidence for this is indirect, however. Furthermore, it is unclear whether pyramidal cells or interneurons (or both) are affected, or how these deficits relate to symptoms. Participants with schizophrenia (Scz, n=108), their relatives (n=57), and controls (n=107) underwent three electroencephalography paradigms – resting, mismatch negativity, and 40 Hz auditory steady-state response – and resting functional magnetic resonance imaging. Dynamic causal modelling was used to quantify synaptic connectivity in cortical microcircuits. Across all four paradigms, characteristic Scz data features were best explained by models with greater self-inhibition (decreased synaptic gain), in pyramidal cells. Furthermore, disinhibition in auditory areas predicted abnormal auditory perception (and positive symptoms) in Scz, in three paradigms. Thus, psychotic symptoms of Scz may result from a downregulation of inhibitory interneurons that may compensate for diminished postsynaptic gain in pyramidal cells.

Functional integration

Active Inference and Cognitive Control: Balancing Deliberation and Habits through Precision Optimization

We advance a novel formulation of cognitive control within the active inference framework. The theory proposes that cognitive control amounts to optimising a precision parameter, which acts as a control signal and balances the contributions of deliberative and habitual components of action selection. To illustrate the theory, we simulate a driving scenario in which the driver follows a well-known route, but encounters unexpected challenges. Our simulations show that a standard active inference model can form adaptive habits; i.e., can pass from deliberative to habitual control when the context is stable, but generally fails to revert to deliberative control, when the context changes. To address this failure of context-sensitivity, we introduce a novel type of hierarchical active inference, in which a lower level is responsible for behavioural control and the higher (or meta-cognitive) level observes the belief updating of the lower level below and is responsible for cognitive control. Crucially, the meta-cognitive level can both form habits and suspend them, by controlling the (precision) parameter that prioritizes deliberative choices at the behavioural level. Furthermore, we show that several processes linked to cognitive control — such as surprise detection, cognitive conflict monitoring, control signal regulation and specification, the simulation of future outcomes and the assessment of the costs of control and mental effort — stem coherently from the free energy minimization scheme that underpins active inference. Finally, we discuss the putative neurobiology of cognitive control by simulating brain dynamics in the mesolimbic and mesocortical pathways of the dopamine system, the dorsal anterior cingulate cortex and the locus coeruleus.

The role of the hippocampus in weighting expectations during inference under uncertainty

Making inference under uncertainty requires an optimal weighting of prior expectations and observations. How this weighting is realized in the brain remains elusive. To investigate this, we recorded functional neuroimaging data while participants estimated a number based on noisy observations. Crucially, the prior expectation about the variability of observations (an expected variability) was manipulated. Consistent with normative models, when novel observations were characterized by higher expected or observed variability, participants' estimates relied more on expectations than novel observations and were characterized by higher stochasticity. Activity in hippocampus increased when novel evidence was characterized by higher expected or observed variability. Response in superior parietal cortex reflected a precision-weighted prediction error signal (i.e., the distance between observations and expectations) that was modulated by hippocampal activity. Our findings implicate the hippocampus during inference under uncertainty, suggesting a role in weighting prior representations over observations and in modulating responsivity of superior parietal cortex to prediction error.

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

Abstract 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.

Posterior probability maps and SPMs

False discovery rate revisited: FDR and topological inference using Gaussian random fields

In this note, we revisit earlier work on false discovery rate (FDR) and evaluate it in relation to topological inference in statistical parametric mapping. We note that controlling the false discovery rate of voxels is not equivalent to controlling the false discovery rate of activations. This is a problem that is unique to inference on images, in which the underlying signal is continuous (i.e., signal which does not have a compact support). In brief, inference based on conventional voxel-wise FDR procedures is not appropriate for inferences on the topological features of a statistical parametric map (SPM), such as peaks or regions of activation. We describe the nature of the problem, illustrate it with some examples and suggest a simple solution based on controlling the false discovery rate of connected excursion sets within an SPM, characterised by their volume.

A Dual Role for Prediction Error in Associative Learning

Confronted with a rich sensory environment, the brain must learn statistical regularities across sensory domains to construct causal models of the world. Here, we used functional magnetic resonance imaging and dynamic causal modeling (DCM) to furnish neurophysiological evidence that statistical associations are learnt, even when task-irrelevant. Subjects performed an audio-visual target-detection task while being exposed to distractor stimuli. Unknown to them, auditory distractors predicted the presence or absence of subsequent visual distractors. We modeled incidental learning of these associations using a Rescorla-Wagner (RW) model. Activity in primary visual cortex and putamen reflected learning-dependent surprise: these areas responded progressively more to unpredicted, and progressively less to predicted visual stimuli. Critically, this prediction-error response was observed even when the absence of a visual stimulus was surprising. We investigated the underlying mechanism by embedding the RW model into a DCM to show that auditory to visual connectivity changed significantly over time as a function of prediction error. Thus, consistent with predictive coding models of perception, associative learning is mediated by prediction-error dependent changes in connectivity. These results posit a dual role for prediction-error in encoding surprise and driving associative plasticity.

Statistical parametric mapping of F-18-DOPA PET

Hallucinations both in and out of context: An active inference account

Hallucinations, including auditory verbal hallucinations (AVH), occur in both the healthy population and in psychotic conditions such as schizophrenia (often developing after a prodromal period). In addition, hallucinations can be in-context (they can be consistent with the environment, such as when one hallucinates the end of a sentence that has been repeated many times), or out-of-context (such as the bizarre hallucinations associated with schizophrenia). In previous work, we introduced a model of hallucinations as false (positive) inferences based on a (Markov decision process) formulation of active inference. In this work, we extend this model to include content-to disclose the computational mechanisms behind in- and out-of-context hallucinations. In active inference, sensory information is used to disambiguate alternative hypotheses about the causes of sensations. Sensory information is balanced against prior beliefs, and when this balance is tipped in the favor of prior beliefs, hallucinations can occur. We show that in-context hallucinations arise when (simulated) subjects cannot use sensory information to correct prior beliefs about hearing a voice, but beliefs about content (i.e. the sequential order of a sentence) remain accurate. When hallucinating subjects also have inaccurate beliefs about state transitions, out-of-context hallucinations occur; i.e. their hallucinated speech content is disordered. Note that out-of-context hallucinations in this setting does not refer to inference about context, but rather to false perceptual inference that emerges when the confidence in-or precision of-sensory evidence is reduced. Furthermore, subjects with inaccurate beliefs about state transitions but an intact ability to use sensory information do not hallucinate and are reminiscent of prodromal patients. This work demonstrates the different computational mechanisms that may underlie the spectrum of hallucinatory experience-from the healthy population to psychotic states.

Exploration, novelty, surprise, and free energy minimization

This paper reviews recent developments under the free energy principle that introduce a normative perspective on classical economic (utilitarian) decision-making based on (active) Bayesian inference. It has been suggested that the free energy principle precludes novelty and complexity, because it assumes that biological systems-like ourselves-try to minimize the long-term average of surprise to maintain their homeostasis. However, recent formulations show that minimizing surprise leads naturally to concepts such as exploration and novelty bonuses. In this approach, agents infer a policy that minimizes surprise by minimizing the difference (or relative entropy) between likely and desired outcomes, which involves both pursuing the goal-state that has the highest expected utility (often termed "exploitation") and visiting a number of different goal-states ("exploration"). Crucially, the opportunity to visit new states increases the value of the current state. Casting decision-making problems within a variational framework, therefore, predicts that our behavior is governed by both the entropy and expected utility of future states. This dissolves any dialectic between minimizing surprise and exploration or novelty seeking.

Active inference, Bayesian optimal design, and expected utility

Active inference, a corollary of the free energy principle, is a formal way of describing the behavior of certain kinds of random dynamical systems that have the appearance of sentience. In this chapter, we describe how active inference combines Bayesian decision theory and optimal Bayesian design principles under a single imperative to minimize expected free energy. It is this aspect of active inference that allows for the natural emergence of information-seeking behavior. When removing prior outcomes preferences from expected free energy, active inference reduces to optimal Bayesian design, i.e., information gain maximization. Conversely, active inference reduces to Bayesian decision theory in the absence of ambiguity and relative risk, i.e., expected utility maximization. Using these limiting cases, we illustrate how behaviors differ when agents select actions that optimize expected utility, expected information gain, and expected free energy. Our T-maze simulations show optimizing expected free energy produces goal-directed information-seeking behavior while optimizing expected utility induces purely exploitive behavior and maximizing information gain engenders intrinsically motivated behavior.

Attention to Action: Specific Modulation of Cortico-Cortical Connectivity Measured Using FMRI

Conference Abstract| August 01 2001 Attention to Action: Specific Modulation of Cortico-Cortical Connectivity Measured Using FMRI Jame B Rowe; Jame B Rowe 1Wellcome Department of Cognitive Neurology, London Search for other works by this author on: This Site PubMed Google Scholar Karl Friston; Karl Friston 1Wellcome Department of Cognitive Neurology, London Search for other works by this author on: This Site PubMed Google Scholar Richard Frackowiak; Richard Frackowiak 1Wellcome Department of Cognitive Neurology, London Search for other works by this author on: This Site PubMed Google Scholar Richard Passingham Richard Passingham 1Wellcome Department of Cognitive Neurology, London Search for other works by this author on: This Site PubMed Google Scholar Clin Sci (Lond) (2001) 101 (s45): 13P. https://doi.org/10.1042/cs101013Pb Views Icon Views Article contents Figures & tables Video Audio Supplementary Data Peer Review Share Icon Share Twitter LinkedIn Cite Icon Cite Get Permissions Citation Jame B Rowe, Karl Friston, Richard Frackowiak, Richard Passingham; Attention to Action: Specific Modulation of Cortico-Cortical Connectivity Measured Using FMRI. Clin Sci (Lond) 1 August 2001; 101 (s45): 13P. doi: https://doi.org/10.1042/cs101013Pb Download citation file: Ris (Zotero) Reference Manager EasyBib Bookends Mendeley Papers EndNote RefWorks BibTex toolbar search Search Dropdown Menu nav search search input Search input auto suggest search filter All ContentAll JournalsClinical Science Search Advanced Search This content is only available as a PDF. © 2001 The Biochemical Society and the Medical Research Society2001 Article PDF first page preview Close Modal You do not currently have access to this content.

Parcels and particles: Markov blankets in the brain

At the inception of human brain mapping, two principles of functional anatomy underwrote most conceptions - and analyses - of distributed brain responses: namely functional segregation and integration. There are currently two main approaches to characterising functional integration. The first is a mechanistic modelling of connectomics in terms of directed effective connectivity that mediates neuronal message passing and dynamics on neuronal circuits. The second phenomenological approach usually characterises undirected functional connectivity (i.e., measurable correlations), in terms of intrinsic brain networks, self-organised criticality, dynamical instability, etc. This paper describes a treatment of effective connectivity that speaks to the emergence of intrinsic brain networks and critical dynamics. It is predicated on the notion of Markov blankets that play a fundamental role in the self-organisation of far from equilibrium systems. Using the apparatus of the renormalisation group, we show that much of the phenomenology found in network neuroscience is an emergent property of a particular partition of neuronal states, over progressively larger scales. As such, it offers a way of linking dynamics on directed graphs to the phenomenology of intrinsic brain networks.

Review for "Predictive processing: is the future just a memory?"

Multi-modal and multi-model interrogation of large-scale functional brain networks

Abstract Current whole-brain models are generally tailored to the modelling of a particular modality of data (e.g., fMRI or MEG/EEG). Although different imaging modalities reflect different aspects of neural activity, we hypothesise that this activity arises from common network dynamics. Building on the universal principles of self-organising delay-coupled nonlinear systems, we aim to link distinct electromagnetic and metabolic features of brain activity to the dynamics on the brain’s macroscopic structural connectome. To jointly predict dynamical and functional connectivity features of distinct signal modalities, we consider two large-scale models generating local short-lived 40 Hz oscillations with various degrees of realism - namely Stuart Landau (SL) and Wilson and Cowan (WC) models. To this end, we measure features of functional connectivity and metastable oscillatory modes (MOMs) in fMRI and MEG signals - and compare them against simulated data. We show that both models can represent MEG functional connectivity (FC) and functional connectivity dynamics (FCD) to a comparable degree, by varying global coupling and mean conduction time delay. For both models, the omission of delays dramatically decreased the performance. For fMRI, the SL model performed worse for FCD, highlighting the importance of balanced dynamics for the emergence of spatiotemporal patterns of ultra-slow dynamics. Notably, optimal working points varied across modalities and no model was able to achieve a correlation with empirical FC higher than 0.45 across modalities for the same set of parameters. Nonetheless, both displayed the emergence of FC patterns beyond the anatomical framework. Finally, we show that both models can generate MOMs with empirical-like properties. Our results demonstrate the emergence of static and dynamic properties of neural activity at different timescales from networks of delay-coupled oscillators at 40 Hz. Given the higher dependence of simulated FC on the underlying structural connectivity, we suggest that mesoscale heterogeneities in neural circuitry may be critical for the emergence of parallel cross-modal functional networks and should be accounted for in future modelling endeavours.