Tracking the unconscious generation of free decisions using ultra-high field fMRI

Recently, we demonstrated using functional magnetic resonance imaging (fMRI) that the outcome of free decisions can be decoded from brain activity several seconds before reaching conscious awareness. Activity patterns in anterior frontopolar cortex (BA 10) were temporally the first to carry intention-related information and thus a candidate region for the unconscious generation of free decisions. In the present study, the original paradigm was replicated and multivariate pattern classification was applied to functional images of frontopolar cortex, acquired using ultra-high field fMRI at 7 Tesla. Here, we show that predictive activity patterns recorded before a decision was made became increasingly stable with increasing temporal proximity to the time point of the conscious decision. Furthermore, detailed questionnaires exploring subjects' thoughts before and during the decision confirmed that decisions were made spontaneously and subjects were unaware of the evolution of their decision outcomes. These results give further evidence that FPC stands at the top of the prefrontal executive hierarchy in the unconscious generation of free decisions.     

Tracking the Unconscious Generation of Free Decisions Using UItra-High Field fMRI

Recently, we demonstrated using functional magnetic resonance imaging (fMRI) that the outcome of free decisions can be decoded from brain activity several seconds before reaching conscious awareness. Activity patterns in anterior frontopolar cortex (BA 10) were temporally the first to carry intention-related information and thus a candidate region for the unconscious generation of free decisions. In the present study, the original paradigm was replicated and multivariate pattern classification was applied to functional images of frontopolar cortex, acquired using ultra-high field fMRI at 7 Tesla. Here, we show that predictive activity patterns recorded before a decision was made became increasingly stable with increasing temporal proximity to the time point of the conscious decision. Furthermore, detailed questionnaires exploring subjects'' thoughts before and during the decision confirmed that decisions were made spontaneously and subjects were unaware of the evolution of their decision outcomes. These results give further evidence that FPC stands at the top of the prefrontal executive hierarchy in the unconscious generation of free decisions.     

The influence of serotonin on fear learning

Learning of associations between aversive stimuli and predictive cues is the basis of Pavlovian fear conditioning and is driven by a mismatch between expectation and outcome. To investigate whether serotonin modulates the formation of such aversive cue-outcome associations, we used functional magnetic resonance imaging (fMRI) and dietary tryptophan depletion to reduce brain serotonin (5-HT) levels in healthy human subjects. In a Pavlovian fear conditioning paradigm, 5-HT depleted subjects compared to a non-depleted control group exhibited attenuated autonomic responses to cues indicating the upcoming of an aversive event. These results were closely paralleled by reduced aversive learning signals in the amygdala and the orbitofrontal cortex, two prominent structures of the neural fear circuit. In agreement with current theories of serotonin as a motivational opponent system to dopamine in fear learning, our data provide first empirical evidence for a role of serotonin in representing formally derived learning signals for aversive events.     

Improvement of Speech Function in Patients with Aphasia: The Right Hemisphere,an Enemy or a Friend?

The purpose of our research is to investigate interhemispheric language functional reorganization in patients with gliomas of the left hemisphere using functional magnetic resonance tomography (fMRI) in comparison with the dynamics of speech disorders. A total of 20 patients with a glioma in the left hemisphere underwent fMRI examination and Luria’s neuropsychological testing. The age of patients varied from 26 to 67 years; the mean age was 40 years (median, interquartile range; 13 women and 7 men). The glioma was located in the frontal lobe (12 patients) 34.50–49.75 years; or in the temporal lobe (8 patients). All patients underwent both fMRI scanning and neuropsychological testing on the same day before the surgery and then 3–10 days and 3, 5–7, 12 months after tumor surgery. The handedness was determined by using self-assessment and the Annett Hand Preference Questionnaire. Almost all the subjects were right-handed, and one was ambidexter. On the basis of the analysis of fMRI data in dynamics, all subjects were divided into two groups: (1) patients with no signs of activation of the right hemisphere homologues of Broca’s and Wernicke’s areas (even in 4 patients with severe aphasia) during the follow-up period (at least one year), and (2) patients with signs of activation in the right-sided Broca’s and Wernicke’s areas, which were found in at least several tests (16 patients; 3 of them had normal speech function during the whole follow-up period). We conclude that the lack of consistency between the presence/absence of aphasia and the activation of homologous speech areas in the right hemisphere in fMRI results from individual differences in the involvement of the right hemisphere in speech processes. Thus, we should be very cautious about the hypothesis of reciprocal relationships of the hemispheres in speech function and the use of this hypothesis in speech rehabilitation.     

Origins of spatial working memory deficits in schizophrenia: an event-related FMRI and near-infrared spectroscopy study

Abnormal prefrontal functioning plays a central role in the working memory (WM) deficits of schizophrenic patients, but the nature of the relationship between WM and prefrontal activation remains undetermined. Using two functional neuroimaging methods, we investigated the neural correlates of remembering and forgetting in schizophrenic and healthy participants. We focused on the brain activation during WM maintenance phase with event-related functional magnetic resonance imaging (fMRI). We also examined oxygenated hemoglobin changes in relation to memory performance with the near-infrared spectroscopy (NIRS) using the same spatial WM task. Distinct types of correct and error trials were segregated for analysis. fMRI data indicated that prefrontal activation was increased during WM maintenance on correct trials in both schizophrenic and healthy subjects. However, a significant difference was observed in the functional asymmetry of frontal activation pattern. Healthy subjects showed increased activation in the right frontal, temporal and cingulate regions. Schizophrenic patients showed greater activation compared with control subjects in left frontal, temporal and parietal regions as well as in right frontal regions. We also observed increased 'false memory' errors in schizophrenic patients, associated with increased prefrontal activation and resembling the activation pattern observed on the correct trials. NIRS data replicated the fMRI results. Thus, increased frontal activity was correlated with the accuracy of WM in both healthy control and schizophrenic participants. The major difference between the two groups concerned functional asymmetry; healthy subjects recruited right frontal regions during spatial WM maintenance whereas schizophrenic subjects recruited a wider network in both hemispheres to achieve the same level of memory performance. Increased "false memory" errors and accompanying bilateral prefrontal activation in schizophrenia suggest that the etiology of memory errors must be considered when comparing group performances. Finally, the concordance of fMRI and NIRS data supports NIRS as an alternative functional neuroimaging method for psychiatric research.     

Effect of acupuncture in mild cognitive impairment and Alzheimer disease: a functional MRI study

We aim to clarify the mechanisms of acupuncture in treating mild cognitive impairment (MCI) and Alzheimer disease (AD) by using functional magnetic resonance imaging (fMRI). Thirty-six right-handed subjects (8 MCI patients, 14 AD patients, and 14 healthy elders) participated in this study. Clinical and neuropsychological examinations were performed on all the subjects. MRI data acquisition was performed on a SIEMENS verio 3-Tesla scanner. The fMRI study used a single block experimental design. We first acquired the baseline resting state data in the initial 3 minutes; we then acquired the fMRI data during the procession of acupuncture stimulation on the acupoints of Tai chong and Hegu for the following 3 minutes. Last, we acquired fMRI data for another 10 minutes after the needle was withdrawn. The preprocessing and data analysis were performed using the statistical parametric mapping (SPM8) software. Then the two-sample t-tests were performed between each two groups of different states. We found that during the resting state, brain activities in AD and MCI patients were different from those of control subjects. During the acupuncture and the second resting state after acupuncture, when comparing to resting state, there are several regions showing increased or decreased activities in MCI, AD subjects compared to normal subjects. Most of the regions were involved in the temporal lobe and the frontal lobe, which were closely related to the memory and cognition. In conclusion, we investigated the effect of acupuncture in AD and MCI patients by combing fMRI and traditional acupuncture. Our fMRI study confirmed that acupuncture at Tai chong (Liv3) and He gu (LI4) can activate certain cognitive-related regions in AD and MCI patients.     

Some Neurophysiological Correlates of Altered Mental States in Labor: Report II. Features of the Superslow Phasic Processes

A group of parturient women (n= 45) was divided into subgroups of subjects with a large and small number of signs of an altered mental state (AMS and NAMS, respectively) during and after labor, according to data of a special psychological questionnaire. The background EEG and the superslow phasic electric processes (SSPP) of the head surface were recorded simultaneously in 16 monopolar leads before and after labor. The parameters of autocorrelation and cross-correlation functions of the processes were calculated. Highly significant differences were found among the subgroups in the parameters of dynamics and spatial synchronization of the SSPP, related, in particular, to the activity of the anterofrontal zones of both hemispheres and of the temporal zones of the right hemisphere. The differences between the AMS and NAMS subgroups were revealed on the basis of the different extents of the unidirectional deviations from the SSPP parameters in the reference group of healthy nulliparous women. The pattern of interrelations of the investigated parameters of the EEG and the SSPP confirms the hypothesis that functional changes in the brain during the adaptation of women to pregnancy termination and physiological labor correlate with a special mental state.     

A Shared Neural Substrate for Mentalizing and the Affective Component of Sentence Comprehension

Using event-related fMRI in a sample of 42 healthy participants, we compared the cerebral activity maps obtained when classifying spoken sentences based on the mental content of the main character (belief, deception or empathy) or on the emotional tonality of the sentence (happiness, anger or sadness). To control for the effects of different syntactic constructions (such as embedded clauses in belief sentences), we subtracted from each map the BOLD activations obtained during plausibility judgments on structurally matching sentences, devoid of emotions or ToM. The obtained theory of mind (ToM) and emotional speech comprehension networks overlapped in the bilateral temporo-parietal junction, posterior cingulate cortex, right anterior temporal lobe, dorsomedial prefrontal cortex and in the left inferior frontal sulcus. These regions form a ToM network, which contributes to the emotional component of spoken sentence comprehension. Compared with the ToM task, in which the sentences were enounced on a neutral tone, the emotional sentence classification task, in which the sentences were play-acted, was associated with a greater activity in the bilateral superior temporal sulcus, in line with the presence of emotional prosody. Besides, the ventromedial prefrontal cortex was more active during emotional than ToM sentence processing. This region may link mental state representations with verbal and prosodic emotional cues. Compared with emotional sentence classification, ToM was associated with greater activity in the caudate nucleus, paracingulate cortex, and superior frontal and parietal regions, in line with behavioral data showing that ToM sentence comprehension was a more demanding task.     

Functional Connectivity in the Brain Estimated by Analysis of Gamma Events

It is known that gamma activity is generated by local networks. In this paper we introduced a new approach for estimation of functional connectivity between neuronal networks by measuring temporal relations between peaks of gamma event amplitudes. We have shown in freely moving rats that gamma events recorded between electrodes 1.5 mm apart in the majority of cases, are generated by different neuronal modules interfering with each other. The map of functional connectivity between brain areas during the resting state, created based on gamma event temporal relationships is in agreement with anatomical connections and with maps described by fMRI methods during the resting state. The transition from the resting state to exploratory activity is accompanied by decreased functional connectivity between most brain areas. Our data suggest that functional connectivity between interhemispheric areas depends on GABAergic transmission, while intrahemispheric functional connectivity is kainate receptor dependent. This approach presents opportunities for merging electrographic and fMRI data on brain functional connectivity in normal and pathological conditions.     

Enhanced tactile performance at the destination of an upcoming saccade

Previous work has demonstrated that upcoming saccades influence visual and auditory performance even for stimuli presented before the saccade is executed. These studies suggest a close relationship between saccade generation and visual/auditory attention. Furthermore, they provide support for Rizzolatti et al.'s premotor model of attention, which suggests that the same circuits involved in motor programming are also responsible for shifts in covert orienting (shifting attention without moving the eyes or changing posture). In a series of experiments, we demonstrate that saccade programming also affects tactile perception. Participants made speeded saccades to the left and right side as well as tactile discriminations of up versus down. The first experiment demonstrates that participants were reliably faster at responding to tactile stimuli near the location of upcoming saccades. In our second experiment, we had the subjects cross their hands and demonstrated that the effect occurs in visual space (rather than the early representations of touch). In our third experiment, the tactile events usually occurred on the opposite side of upcoming eye movement. We found that the benefit at the saccade target location vanished, suggesting that this shift is not obligatory but that it may be vetoed on the basis of expectation.     

Predicting decisions in human social interactions using real-time fMRI and pattern classification

Negotiation and trade typically require a mutual interaction while simultaneously resting in uncertainty which decision the partner ultimately will make at the end of the process. Assessing already during the negotiation in which direction one's counterpart tends would provide a tremendous advantage. Recently, neuroimaging techniques combined with multivariate pattern classification of the acquired data have made it possible to discriminate subjective states of mind on the basis of their neuronal activation signature. However, to enable an online-assessment of the participant's mind state both approaches need to be extended to a real-time technique. By combining real-time functional magnetic resonance imaging (fMRI) and online pattern classification techniques, we show that it is possible to predict human behavior during social interaction before the interacting partner communicates a specific decision. Average accuracy reached approximately 70% when we predicted online the decisions of volunteers playing the ultimatum game, a well-known paradigm in economic game theory. Our results demonstrate the successful online analysis of complex emotional and cognitive states using real-time fMRI, which will enable a major breakthrough for social fMRI by providing information about mental states of partners already during the mutual interaction. Interestingly, an additional whole brain classification across subjects confirmed the online results: anterior insula, ventral striatum, and lateral orbitofrontal cortex, known to act in emotional self-regulation and reward processing for adjustment of behavior, appeared to be strong determinants of later overt behavior in the ultimatum game. Using whole brain classification we were also able to discriminate between brain processes related to subjective emotional and motivational states and brain processes related to the evaluation of objective financial incentives.     

Eye Movements Provide an Index of Veridical Memory for Temporal Order

The present research examined whether eye movements during retrieval capture the relation between an event and its temporal attributes. In two experiments (N=76), we found converging evidence that eye movements reflected the veridicality of memory for temporal order seconds before overt memory judgments, suggesting that these movements captured indirect access to temporal information. These eye movements did not entirely depend on the amount of contextual cueing available (Experiment 1) and reflected the unique ordinal position of an event in a sequence (Experiment 2). Based on our results, we conclude that eye movements reflected the absolute temporal order of past events.     

Asymmetrical activation in the human brain during processing of fearful faces

Traditional split-field studies and patient research indicate a privileged role for the right hemisphere in emotional processing [1-7], but there has been little direct fMRI evidence for this, despite many studies on emotional-face processing [8-10](see Supplemental Background). With fMRI, we addressed differential hemispheric processing of fearful versus neutral faces by presenting subjects with faces bilaterally [11-13]and orthogonally manipulating whether each hemifield showed a fearful or neutral expression prior to presentation of a checkerboard target. Target discrimination in the left visual field was more accurate after a fearful face was presented there. Event-related fMRI showed right-lateralized brain activations for fearful minus neutral left-hemifield faces in right visual areas, as well as more activity in the right than in the left amygdala. These activations occurred regardless of the type of right-hemifield face shown concurrently, concordant with the behavioral effect. No analogous behavioral or fMRI effects were observed for fearful faces in the right visual field (left hemisphere). The amygdala showed enhanced functional coupling with right-middle and anterior-fusiform areas in the context of a left-hemifield fearful face. These data provide behavioral and fMRI evidence for right-lateralized emotional processing during bilateral stimulation involving enhanced coupling of the amygdala and right-hemispheric extrastriate cortex.     

Neonatal brain injury and neuroanatomy of memory processing following very preterm birth in adulthood: an fMRI study

Altered functional neuroanatomy of high-order cognitive processing has been described in very preterm individuals (born before 33 weeks of gestation; VPT) compared to controls in childhood and adolescence. However, VPT birth may be accompanied by different types of adverse neonatal events and associated brain injury, the severity of which may have differential effects on brain development and subsequent neurodevelopmental outcome. We conducted a functional magnetic resonance imaging (fMRI) study to investigate how differing degrees of neonatal brain injury, detected by neonatal ultrasounds, affect the functional neuroanatomy of memory processing in VPT young adults. We used a verbal paired associates learning task, consisting of four encoding, four cued-recall and four baseline condition blocks. To further investigate whether differences in neural activation between the groups were modulated by structural brain changes, structural MRI data were also collected. We studied 12 VPT young adults with a history of periventricular haemorrhage with associated ventricular dilatation, 17 VPT individuals with a history of uncomplicated periventricular haemorrhage, 12 individuals with normal ultrasonographic findings, and 17 controls. Results of a linear trend analysis demonstrated that during completion of the paired associates learning task right frontal and right parietal brain activation decreased as the severity of neonatal brain injury increased. There were no statistically significant between-group differences in on-line task performance and participants' intelligence quotient (IQ) at assessment. This pattern of differential activation across the groups was observed particularly in the right middle frontal gyrus during encoding and in the right posterior cingulate gyrus during recall. Structural MRI data analysis revealed that grey matter volume in the right superior temporal gyrus, right cerebellum, left middle temporal gyrus, right globus pallidus and right medial frontal gyrus decreased with increasing severity of neonatal brain injury. However, the significant between-group functional neuroanatomical differences were not directly attributable to the detected structural regional differences.     

Consistency of network modules in resting-state FMRI connectome data

At rest, spontaneous brain activity measured by fMRI is summarized by a number of distinct resting state networks (RSNs) following similar temporal time courses. Such networks have been consistently identified across subjects using spatial ICA (independent component analysis). Moreover, graph theory-based network analyses have also been applied to resting-state fMRI data, identifying similar RSNs, although typically at a coarser spatial resolution. In this work, we examined resting-state fMRI networks from 194 subjects at a voxel-level resolution, and examined the consistency of RSNs across subjects using a metric called scaled inclusivity (SI), which summarizes consistency of modular partitions across networks. Our SI analyses indicated that some RSNs are robust across subjects, comparable to the corresponding RSNs identified by ICA. We also found that some commonly reported RSNs are less consistent across subjects. This is the first direct comparison of RSNs between ICAs and graph-based network analyses at a comparable resolution.     

Physiological correlates of individual differences in decision-making time during purposeful mental activity in humans

EEG correlates of individual differences in decision-making time were studied in subjects performing the task of memorizing and subsequently reproducing, on a monitor screen, a sequence of signals. Forty-six students were volunteers in the study, carried out with the use of an original computer-aided technique. Pioneering data on the individual specificity of physiological processes underlying human mental activity were obtained. Individual differences in EEG characteristics related to differences in the temporal parameters of the decision-making stage were found. In a situation directly preceding the activity, subjects characterized by a short decision-making time exhibited higher powers of the Δ (in the occipital, parietal, and central cortical areas) and θ-(in both the central and the right frontal and temporal areas) EEG rhythms. The subjects with a short decision-making time differed from those with a long decision-making time in a higher power of the θ rhythm in the right temporal area during memorization and an increased θ rhythm power in the frontal areas during reproduction of a signal sequence.     

Neural Correlates of Belief and Emotion Attribution in Schizophrenia

Impaired mental state attribution is a core social cognitive deficit in schizophrenia. With functional magnetic resonance imaging (fMRI), this study examined the extent to which the core neural system of mental state attribution is involved in mental state attribution, focusing on belief attribution and emotion attribution. Fifteen schizophrenia outpatients and 14 healthy controls performed two mental state attribution tasks in the scanner. In a Belief Attribution Task, after reading a short vignette, participants were asked infer either the belief of a character (a false belief condition) or a physical state of an affair (a false photograph condition). In an Emotion Attribution Task, participants were asked either to judge whether character(s) in pictures felt unpleasant, pleasant, or neutral emotion (other condition) or to look at pictures that did not have any human characters (view condition). fMRI data were analyzing focusing on a priori regions of interest (ROIs) of the core neural systems of mental state attribution: the medial prefrontal cortex (mPFC), temporoparietal junction (TPJ) and precuneus. An exploratory whole brain analysis was also performed. Both patients and controls showed greater activation in all four ROIs during the Belief Attribution Task than the Emotion Attribution Task. Patients also showed less activation in the precuneus and left TPJ compared to controls during the Belief Attribution Task. No significant group difference was found during the Emotion Attribution Task in any of ROIs. An exploratory whole brain analysis showed a similar pattern of neural activations. These findings suggest that while schizophrenia patients rely on the same neural network as controls do when attributing beliefs of others, patients did not show reduced activation in the key regions such as the TPJ. Further, this study did not find evidence for aberrant neural activation during emotion attribution or recruitment of compensatory brain regions in schizophrenia.     

Uncovering the spatio-temporal dynamics of value-based decision-making in the human brain: a combined fMRI–EEG study

While there is a growing body of functional magnetic resonance imaging (fMRI) evidence implicating a corpus of brain regions in value-based decision-making in humans, the limited temporal resolution of fMRI cannot address the relative temporal precedence of different brain regions in decision-making. To address this question, we adopted a computational model-based approach to electroencephalography (EEG) data acquired during a simple binary choice task. fMRI data were also acquired from the same participants for source localization. Post-decision value signals emerged 200 ms post-stimulus in a predominantly posterior source in the vicinity of the intraparietal sulcus and posterior temporal lobe cortex, alongside a weaker anterior locus. The signal then shifted to a predominantly anterior locus 850 ms following the trial onset, localized to the ventromedial prefrontal cortex and lateral prefrontal cortex. Comparison signals between unchosen and chosen options emerged late in the trial at 1050 ms in dorsomedial prefrontal cortex, suggesting that such comparison signals may not be directly associated with the decision itself but rather may play a role in post-decision action selection. Taken together, these results provide us new insights into the temporal dynamics of decision-making in the brain, suggesting that for a simple binary choice task, decisions may be encoded predominantly in posterior areas such as intraparietal sulcus, before shifting anteriorly.     

Visual Benefits in Apparent Motion Displays: Automatically Driven Spatial and Temporal Anticipation Are Partially Dissociated

Many behaviourally relevant sensory events such as motion stimuli and speech have an intrinsic spatio-temporal structure. This will engage intentional and most likely unintentional (automatic) prediction mechanisms enhancing the perception of upcoming stimuli in the event stream. Here we sought to probe the anticipatory processes that are automatically driven by rhythmic input streams in terms of their spatial and temporal components. To this end, we employed an apparent visual motion paradigm testing the effects of pre-target motion on lateralized visual target discrimination. The motion stimuli either moved towards or away from peripheral target positions (valid vs. invalid spatial motion cueing) at a rhythmic or arrhythmic pace (valid vs. invalid temporal motion cueing). Crucially, we emphasized automatic motion-induced anticipatory processes by rendering the motion stimuli non-predictive of upcoming target position (by design) and task-irrelevant (by instruction), and by creating instead endogenous (orthogonal) expectations using symbolic cueing. Our data revealed that the apparent motion cues automatically engaged both spatial and temporal anticipatory processes, but that these processes were dissociated. We further found evidence for lateralisation of anticipatory temporal but not spatial processes. This indicates that distinct mechanisms may drive automatic spatial and temporal extrapolation of upcoming events from rhythmic event streams. This contrasts with previous findings that instead suggest an interaction between spatial and temporal attention processes when endogenously driven. Our results further highlight the need for isolating intentional from unintentional processes for better understanding the various anticipatory mechanisms engaged in processing behaviourally relevant stimuli with predictable spatio-temporal structure such as motion and speech.     

The spatial structure of the alpha rhythm in the healthy human being studied by EEG mapping]

EEG study was conducted in the state of relative rest in 15 healthy subjects with predominance of the alpha rhythm. Data processing was performed on neuromapper ("Neuroscience", Great Britain). Principal attention was paid to the dynamics of spatial-temporal relations of the alpha rhythm. Cyclic changes were shown of the alpha-rhythm amplitude, proceeding with change of high and low amplitudes during seconds, varying in time in various individuals. Three types of spatial distribution of the alpha rhythm over the cortex at the relative rest were obtained: 1) generalized distribution over the cortex with the wavy shift of the frequency fields; 2) formation of delimited local zones of the alpha rhythm, differing by the frequency from the rhythm in other cortical areas; 3) local zone of the low-frequency alpha rhythm in the visual projection zone (18 and 19 fields). Change of the distribution types of the alpha rhythm in the state of rest takes place in the seconds of time intervals, corresponding, according to the literature data, to the proceeding of elementary mental processes.