Ryszard Auksztulewicz

Causal Role of Dorsolateral Prefrontal Cortex in Human Perceptual Decision Making

The way that we interpret and interact with the world entails making decisions on the basis of available sensory evidence. Recent primate neurophysiology [1-6], human neuroimaging [7-13], and modeling experiments [14-19] have demonstrated that perceptual decisions are based on an integrative process in which sensory evidence accumulates over time until an internal decision bound is reached. Here we used repetitive transcranial magnetic stimulation (rTMS) to provide causal support for the role of the dorsolateral prefrontal cortex (DLPFC) in this integrative process. Specifically, we used a speeded perceptual categorization task designed to induce a time-dependent accumulation of sensory evidence through rapidly updating dynamic stimuli and found that disruption of the left DLPFC with low-frequency rTMS reduced accuracy and increased response times relative to a sham condition. Importantly, using the drift-diffusion model, we show that these behavioral effects correspond to a decrease in drift rate, a parameter describing the rate and thereby the efficiency of the sensory evidence integration in the decision process. These results provide causal evidence linking the DLPFC to the mechanism of evidence accumulation during perceptual decision making.

Attentional Enhancement of Auditory Mismatch Responses: a DCM/MEG Study

Despite similar behavioral effects, attention and expectation influence evoked responses differently: Attention typically enhances event-related responses, whereas expectation reduces them. This dissociation has been reconciled under predictive coding, where prediction errors are weighted by precision associated with attentional modulation. Here, we tested the predictive coding account of attention and expectation using magnetoencephalography and modeling. Temporal attention and sensory expectation were orthogonally manipulated in an auditory mismatch paradigm, revealing opposing effects on evoked response amplitude. Mismatch negativity (MMN) was enhanced by attention, speaking against its supposedly pre-attentive nature. This interaction effect was modeled in a canonical microcircuit using dynamic causal modeling, comparing models with modulation of extrinsic and intrinsic connectivity at different levels of the auditory hierarchy. While MMN was explained by recursive interplay of sensory predictions and prediction errors, attention was linked to the gain of inhibitory interneurons, consistent with its modulation of sensory precision.

Repetition suppression and its contextual determinants in predictive coding

This paper presents a review of theoretical and empirical work on repetition suppression in the context of predictive coding. Predictive coding is a neurobiologically plausible scheme explaining how biological systems might perform perceptual inference and learning. From this perspective, repetition suppression is a manifestation of minimising prediction error through adaptive changes in predictions about the content and precision of sensory inputs. Simulations of artificial neural hierarchies provide a principled way of understanding how repetition suppression – at different time scales – can be explained in terms of inference and learning implemented under predictive coding. This formulation of repetition suppression is supported by results of numerous empirical studies of repetition suppression and its contextual determinants.

Recurrent Neural Processing and Somatosensory Awareness

The neural mechanisms of stimulus detection, despite extensive research, remain elusive. The recurrent processing hypothesis, a prominent theoretical account of perceptual awareness, states that, although stimuli might in principle evoke feedforward activity propagating through the visual cortex, stimuli that become consciously detected are further processed in feedforward–feedback loops established between cortical areas. To test this theory in the tactile modality, we applied dynamic causal modeling to electroencephalography (EEG) data acquired from humans in a somatosensory detection task. In the analysis of stimulation-induced event-related potentials (ERPs), we focused on model-based evidence for feedforward, feedback, and recurrent processing between primary and secondary somatosensory cortices. Bayesian model comparison revealed that, although early EEG components were well explained by both the feedforward and the recurrent models, the recurrent model outperformed the other models when later EEG segments were analyzed. Within the recurrent model, stimulus detection was characterized by a relatively early strength increase of the feedforward connection from primary to secondary somatosensory cortex (>80 ms). At longer latencies (>140 ms), also the feedback connection showed a detection-related strength increase. The modeling results on relative evidence between recurrent and feedforward model comparison support the hypothesis that the ERP responses from sensory areas arising after aware stimulus detection can be explained by increased recurrent processing within the somatosensory network in the later stages of stimulus processing.

Subjective Rating of Weak Tactile Stimuli Is Parametrically Encoded in Event-Related Potentials

Neural signatures of somatosensory awareness have often been studied by examining EEG responses to hardly detectable stimuli. Previous reports consistently showed that event-related potentials (ERPs) measured over early somatosensory cortex diverge for detected and missed perithreshold stimuli at 80–100 ms after stimulus onset. So far, however, all previous studies have operationalized somatosensory awareness as binary stimulus detection. Here, we investigated whether ERP components attributed to neuronal activity in early somatosensory cortices would parametrically reflect subjective ratings of stimulus awareness. EEG (64 channel) was recorded in human participants (N = 20), with perithreshold electrical stimulation applied to the left median nerve. Participants indicated perceptibility on a continuous visual rating scale, and stimulation intensity was readjusted in each block to a perithreshold level. The aim of the analysis was to investigate which brain areas reflect the subsequent perceptual awareness ratings parametrically, and how early such parametric effects occur. Parametric ERP effects were found as early as 86 ms after stimulus onset. This parametric modulation of ERP amplitude was source localized to secondary somatosensory cortex, and attributed to feedforward processing between primary and secondary somatosensory cortex by means of dynamic causal modeling (DCM). Furthermore, later in the analysis window, the subjective rating of stimuli correlated with the amplitude of the N140 component and with a broadly distributed P300 component. By DCM modeling, these late effects were explained in terms of recurrent processing within the network of somatosensory and premotor cortices. Our results indicate that early neural activity in the somatosensory cortex can reflect the subjective quality of tactile perception.

Maintenance and manipulation of somatosensory information in ventrolateral prefrontal cortex.

Neuroimaging studies of working memory (WM) suggest that prefrontal cortex may assist sustained maintenance, but also internal manipulation, of stimulus representations in lower‐level areas. A different line of research in the somatosensory domain indicates that neuronal activity in ventrolateral prefrontal cortex (VLPFC) may also represent specific memory contents in itself, however leaving open to what extent top‐down control on lower‐level areas is exerted, or how internal manipulation processes are implemented. We used functional imaging and connectivity analysis to study static maintenance and internal manipulation of tactile working memory contents after physically identical stimulation conditions, in human subjects. While both tasks recruited similar subareas in the inferior frontal gyrus (IFG) in VLPFC, static maintenance of the tactile information was additionally characterized by increased functional coupling between IFG and primary somatosensory cortex. Independently, during internal manipulation, a quantitative representation of the task‐relevant information was evident in IFG itself, even in the absence of physical stimulation. Together, these findings demonstrate the functional diversity of activity within VLPFC according to different working memory demands, and underline the role of IFG as a core region in sensory WM processing. Hum Brain Mapp 35:2412–2423, 2014.

Impairing somatosensory working memory using rTMS.

Numerous studies in animals and humans have related central aspects of somatosensory working memory function to neural activity in the inferior frontal gyrus (IFG). However, as previous studies have almost exclusively used correlational analyses, the question whether sustained neural activity in the IFG is causally involved in successful maintenance of somatosensory information remains unanswered. We used an online repetitive transcranial magnetic stimulation (rTMS) protocol to disrupt neuronal activity in the IFG while participants were maintaining tactile information throughout the delay for later comparison against a probe stimulus. rTMS impaired participants’ performance in the working memory task, but not in a physically matched perceptual control task. Targeting the IFG in either hemisphere led to comparable working memory impairment. Our results show that the neural activity in the IFG plays a causal role in successful maintenance of somatosensory information.

Expectation violation and attention to pain jointly modulate neural gain in somatosensory cortex

Abstract The neural processing and experience of pain are influenced by both expectations and attention. For example, the amplitude of event‐related pain responses is enhanced by both novel and unexpected pain, and by moving the focus of attention towards a painful stimulus. Under predictive coding, this congruence can be explained by appeal to a precision‐weighting mechanism, which mediates bottom‐up and top‐down attentional processes by modulating the influence of feedforward and feedback signals throughout the cortical hierarchy. The influence of expectation and attention on pain processing can be mapped onto changes in effective connectivity between or within specific neuronal populations, using a canonical microcircuit (CMC) model of hierarchical processing. We thus implemented a CMC within dynamic causal modelling for magnetoencephalography in human subjects, to investigate how expectation violation and attention to pain modulate intrinsic (within‐source) and extrinsic (between‐source) connectivity in the somatosensory hierarchy. This enabled us to establish whether both expectancy and attentional processes are mediated by a similar precision‐encoding mechanism within a network of somatosensory, frontal and parietal sources. We found that both unexpected and attended pain modulated the gain of superficial pyramidal cells in primary and secondary somatosensory cortex. This modulation occurred in the context of increased lateralized recurrent connectivity between somatosensory and fronto‐parietal sources, driven by unexpected painful occurrences. Finally, the strength of effective connectivity parameters in S1, S2 and IFG predicted individual differences in subjective pain modulation ratings. Our findings suggest that neuromodulatory gain control in the somatosensory hierarchy underlies the influence of both expectation violation and attention on cortical processing and pain perception. HighlightsExpectation and attention influence how pain is processed and perceived.Pain‐related signals are processed throughout a hierarchy of somatosensory and fronto‐parietal regions.Expectation violation and attention to pain modulate intrinsic and extrinsic connectivity in the somatosensory hierarchy.Both expectation violation and attention change the precision of pain‐related signals in S1 and S2.Intrinsic and extrinsic connectivity parameters predicted subjective pain modulation ratings.

Task relevance modulates the behavioural and neural effects of sensory predictions

The brain is thought to generate internal predictions to optimize behaviour. However, it is unclear whether predictions signalling is an automatic brain function or depends on task demands. Here, we manipulated the spatial/temporal predictability of visual targets, and the relevance of spatial/temporal information provided by auditory cues. We used magnetoencephalography (MEG) to measure participants’ brain activity during task performance. Task relevance modulated the influence of predictions on behaviour: spatial/temporal predictability improved spatial/temporal discrimination accuracy, but not vice versa. To explain these effects, we used behavioural responses to estimate subjective predictions under an ideal-observer model. Model-based time-series of predictions and prediction errors (PEs) were associated with dissociable neural responses: predictions correlated with cue-induced beta-band activity in auditory regions and alpha-band activity in visual regions, while stimulus-bound PEs correlated with gamma-band activity in posterior regions. Crucially, task relevance modulated these spectral correlates, suggesting that current goals influence PE and prediction signalling.

The influence of spontaneous brain oscillations on apparent motion perception

A good example of inferential processes in perception is long-range apparent motion (AM), the illusory percept of visual motion that occurs when two spatially distinct stationary visual objects are presented in alternating sequence. The AM illusion is strongest at presentation frequencies around 3 Hz. At lower presentation frequencies, the percept varies from trial to trial between AM and sequential alternation, while at higher frequencies perception varies between AM and two simultaneously flickering objects. Previous studies have demonstrated that prestimulus alpha oscillations explain trial-to-trial variability in detection performance for visual stimuli presented at threshold. In the present study, we investigated whether fluctuations of prestimulus alpha oscillations can also account for variations in AM perception. Prestimulus alpha power was stronger when observers reported AM perception in subsequent trials with low presentation frequencies, while at high presentation frequencies there were no significant differences in alpha power preceding AM and veridical flicker perception. Moreover, when observers perceived AM the prestimulus functional connectivity between frontal and occipital channels was increased in the alpha band, as revealed by the imaginary part of coherency, which is insensitive to artefacts from volume conduction. Dynamic causal modelling of steady-state responses revealed that the most likely direction of this fronto-occipital connectivity was from frontal to occipital sources. These results point to a role of ongoing alpha oscillations in the inferential process that gives rise to the perception of AM and suggest that fronto-occipital interactions bias perception towards internally generated predictions.