Floris P. de Lange

Expectation in perceptual decision making: neural and computational mechanisms

Sensory signals are highly structured in both space and time. These structural regularities in visual information allow expectations to form about future stimulation, thereby facilitating decisions about visual features and objects. Here, we discuss how expectation modulates neural signals and behaviour in humans and other primates. We consider how expectations bias visual activity before a stimulus occurs, and how neural signals elicited by expected and unexpected stimuli differ. We discuss how expectations may influence decision signals at the computational level. Finally, we consider the relationship between visual expectation and related concepts, such as attention and adaptation.

Neural Topography and Content of Movement Representations

We have used implicit motor imagery to investigate the neural correlates of motor planning independently from actual movements. Subjects were presented with drawings of left or right hands and asked to judge the hand laterality, regardless of the stimulus rotation from its upright orientation. We paired this task with a visual imagery control task, in which subjects were presented with typographical characters and asked to report whether they saw a canonical letter or its mirror image, regardless of its rotation. We measured neurovascular activity with fast event-related fMRI, distinguishing responses parametrically related to motor imagery from responses evoked by visual imagery and other task-related phenomena. By quantifying behavioral and neurovascular correlates of imagery on a trial-by-trial basis, we could discriminate between stimulus-related, mental rotation-related, and response-related neural activity. We found that specific portions of the posterior parietal and precentral cortex increased their activity as a function of mental rotation only during the motor imagery task. Within these regions, the parietal cortex was visually responsive, whereas the dorsal precentral cortex was not. Response- but not rotation-related activity was found around the left central sulcus (putative primary motor cortex) during both imagery tasks. Our study provides novel evidence on the topography and content of movement representations in the human brain. During intended action, the posterior parietal cortex combines somatosensory and visuomotor information, whereas the dorsal premotor cortex generates the actual motor plan, and the primary motor cortex deals with movement execution. We discuss the relevance of these results in the context of current models of action planning.

Increase in prefrontal cortical volume following cognitive behavioural therapy in patients with chronic fatigue syndrome

Chronic fatigue syndrome (CFS) is a disabling disorder, characterized by persistent or relapsing fatigue. Recent studies have detected a decrease in cortical grey matter volume in patients with CFS, but it is unclear whether this cerebral atrophy constitutes a cause or a consequence of the disease. Cognitive behavioural therapy (CBT) is an effective behavioural intervention for CFS, which combines a rehabilitative approach of a graded increase in physical activity with a psychological approach that addresses thoughts and beliefs about CFS which may impair recovery. Here, we test the hypothesis that cerebral atrophy may be a reversible state that can ameliorate with successful CBT. We have quantified cerebral structural changes in 22 CFS patients that underwent CBT and 22 healthy control participants. At baseline, CFS patients had significantly lower grey matter volume than healthy control participants. CBT intervention led to a significant improvement in health status, physical activity and cognitive performance. Crucially, CFS patients showed a significant increase in grey matter volume, localized in the lateral prefrontal cortex. This change in cerebral volume was related to improvements in cognitive speed in the CFS patients. Our findings indicate that the cerebral atrophy associated with CFS is partially reversed after effective CBT. This result provides an example of macroscopic cortical plasticity in the adult human brain, demonstrating a surprisingly dynamic relation between behavioural state and cerebral anatomy. Furthermore, our results reveal a possible neurobiological substrate of psychotherapeutic treatment.

Gray matter volume reduction in the chronic fatigue syndrome

The chronic fatigue syndrome (CFS) is a disabling disorder of unknown etiology. The symptomatology of CFS (central fatigue, impaired concentration, attention and memory) suggests that this disorder could be related to alterations at the level of the central nervous system. In this study, we have used an automated and unbiased morphometric technique to test whether CFS patients display structural cerebral abnormalities. We mapped structural cerebral morphology and volume in two cohorts of CFS patients (in total 28 patients) and healthy controls (in total 28 controls) from high-resolution structural magnetic resonance images, using voxel-based morphometry. Additionally, we recorded physical activity levels to explore the relation between severity of CFS symptoms and cerebral abnormalities. We observed significant reductions in global gray matter volume in both cohorts of CFS patients, as compared to matched control participants. Moreover, the decline in gray matter volume was linked to the reduction in physical activity, a core aspect of CFS. These findings suggest that the central nervous system plays a key role in the pathophysiology of CFS and point to a new objective and quantitative tool for clinical diagnosis of this disabling disorder.

Motor imagery: a window into the mechanisms and alterations of the motor system.

Motor imagery is a widely used paradigm for the study of cognitive aspects of action control, both in the healthy and the pathological brain. In this paper we review how motor imagery research has advanced our knowledge of behavioral and neural aspects of action control, both in healthy subjects and clinical populations. Furthermore, we will illustrate how motor imagery can provide new insights in a poorly understood psychopathological condition: conversion paralysis (CP). We measured behavioral and cerebral responses with functional magnetic resonance imaging (fMRI) in seven CP patients with a lateralized paresis of the arm as they imagined moving the affected or the unaffected hand. Imagined actions were either implicitly induced by the task requirements, or explicitly instructed through verbal instructions. We previously showed that implicitly induced motor imagery of the affected limb leads to larger ventromedial prefrontal responses compared to motor imagery of the unaffected limb. We interpreted this effect in terms of greater self-monitoring of actions during motor imagery of the affected limb. Here, we report new data in support of this interpretation: inducing self-monitoring of actions of both the affected and the unaffected limb (by means of explicitly cued motor imagery) abolishes the activation difference between the affected and the unaffected hand in the ventromedial prefrontal cortex. Our results show that although implicit and explicit motor imagery both entail motor simulations, they differ in terms of the amount of action monitoring they induce. The increased self-monitoring evoked by explicit motor imagery can have profound cerebral consequences in a psychopathological condition.

Cerebral compensation during motor imagery in Parkinson's disease.

In neurodegenerative disorders, neural damage can trigger compensatory mechanisms that minimize behavioural impairments. Here, we aimed at characterizing cerebral compensation during motor imagery in Parkinsons disease (PD), while controlling for altered motor execution and sensory feedback. We used a within-patient design to compare the most and least affected hand in 19 right-handed PD patients with markedly right-lateralized symptoms. We used a motor imagery (MI) task in which the patients were required to judge the laterality of hand images, rotated either in a lateral or in a medial orientation with respect to the body sagittal plane. This design allowed us to compare cerebral activity (using fMRI) evoked by MI of each hand separately, while objectively monitoring task performance. Reaction times and parieto-premotor activity increased in a similar manner as a function of stimulus rotation during motor imagery of left and right hands. However, patients were markedly slower when judging images of the affected hand in lateral orientations, and there was a corresponding increase in activity in the right extrastriate body area (EBA) and occipito-parietal cortex during mental rotation of the affected hand. Furthermore, these regions increased their connectivity towards the left PMd for right (affected) hands in a lateral orientation. We infer that, in strongly lateralized PD patients, motor imagery of the most-affected hand exploits additional resources in extrastriate visual areas. These findings characterize the cerebral bases of the increased dependence on visual information processing during the generation of motor plans in PD, pointing to its compensatory role.

Interactions between posterior gamma and frontal alpha/beta oscillations during imagined actions

Several studies have revealed that posterior parietal and frontal regions support planning of hand movements but far less is known about how these cortical regions interact during the mental simulation of a movement. Here, we have used magnetoencephalography (MEG) to investigate oscillatory interactions between posterior and frontal areas during the performance of a well-established motor imagery task that evokes motor simulation: mental rotation of hands. Motor imagery induced sustained power suppression in the alpha and beta band over the precentral gyrus and a power increase in the gamma band over bilateral occipito-parietal cortex. During motor imagery of left hand movements, there was stronger alpha and beta band suppression over the right precentral gyrus. The duration of these power changes increased, on a trial-by-trial basis, as a function of the motoric complexity of the imagined actions. Crucially, during a specific period of the movement simulation, the power fluctuations of the frontal beta-band oscillations became coupled with the occipito-parietal gamma-band oscillations. Our results provide novel information about the oscillatory brain activity of posterior and frontal regions. The persistent functional coupling between these regions during task performance emphasizes the importance of sustained interactions between frontal and occipito-parietal areas during mental simulation of action.

Repetition Suppression and Expectation Suppression Are Dissociable in Time in Early Auditory Evoked Fields

Repetition of a stimulus, as well as valid expectation that a stimulus will occur, both attenuate the neural response to it. These effects, repetition suppression and expectation suppression, are typically confounded in paradigms in which the nonrepeated stimulus is also relatively rare (e.g., in oddball blocks of mismatch negativity paradigms, or in repetition suppression paradigms with multiple repetitions before an alternation). However, recent hierarchical models of sensory processing inspire the hypothesis that the two might be separable in time, with repetition suppression occurring earlier, as a consequence of local transition probabilities, and suppression by expectation occurring later, as a consequence of learnt statistical regularities. Here we test this hypothesis in an auditory experiment by orthogonally manipulating stimulus repetition and stimulus expectation and, using magnetoencephalography, measuring the neural response over time in human subjects. We found that stimulus repetition (but not stimulus expectation) attenuates the early auditory response (40–60 ms), while stimulus expectation (but not stimulus repetition) attenuates the subsequent, intermediate stage of auditory processing (100–200 ms). These findings are well in line with hierarchical predictive coding models, which posit sequential stages of prediction error resolution, contingent on the level at which the hypothesis is generated.

How Prediction Errors Shape Perception, Attention, and Motivation

Prediction errors (PE) are a central notion in theoretical models of reinforcement learning, perceptual inference, decision-making and cognition, and prediction error signals have been reported across a wide range of brain regions and experimental paradigms. Here, we will make an attempt to see the forest for the trees and consider the commonalities and differences of reported PE signals in light of recent suggestions that the computation of PE forms a fundamental mode of brain function. We discuss where different types of PE are encoded, how they are generated, and the different functional roles they fulfill. We suggest that while encoding of PE is a common computation across brain regions, the content and function of these error signals can be very different and are determined by the afferent and efferent connections within the neural circuitry in which they arise.

The suppression of repetition enhancement: A review of fMRI studies

Repetition suppression in fMRI studies is generally thought to underlie behavioural facilitation effects (i.e., priming) and it is often used to identify the neuronal representations associated with a stimulus. However, this pays little heed to the large number of repetition enhancement effects observed under similar conditions. In this review, we identify several cognitive variables biasing repetition effects in the BOLD response towards enhancement instead of suppression. These variables are stimulus recognition, learning, attention, expectation and explicit memory. We also evaluate which models can account for these repetition effects and come to the conclusion that there is no one single model that is able to embrace all repetition enhancement effects. Accumulation, novel network formation as well as predictive coding models can all explain subsets of repetition enhancement effects.