SUMMARY Human recognition performance is characterized by abrupt changes in perceptual states. Understanding the neuronal dynamics underlying such transitions could provide important insights into mechanisms of recognition and perceptual awareness. Here we examined patients monitored for clinical purposes with multiple subdural electrodes. The patients participated in a backward masking experiment in which pictures of various object categories were presented briefly followed by a mask. We recorded ECoG from 445 electrodes placed in 11 patients. We found a striking increase in gamma power (30–70 Hz) and evoked responses specifically associated with successful recognition. The enhanced activation occurred 150–200 ms after stimulus onset and consistently outlasted the stimulus presentation. We propose that the gamma and evoked potential activations reflect a rapid increase in recurrent neuronal activity that plays a critical role in the emergence of a recognizable visual percept in conscious awareness.
Recent advances in blood oxygen level-dependent-functional MRI (BOLD-fMRI)-based neurofeedback reveal that participants can modulate neuronal properties. However, it is unknown whether such training effects can be introduced in the absence of participants' awareness that they are being trained. Here, we show unconscious neurofeedback training, which consequently produced changes in functional connectivity, introduced in participants who received positive and negative rewards that were covertly coupled to activity in two category-selective visual cortex regions. The results indicate that brain networks can be modified even in the complete absence of intention and awareness of the learning situation, raising intriguing possibilities for clinical interventions.neurofeedback | training | reward | spontaneous activity | functional connectivity T here has been a growing interest in the field of neuroscience in the use of neurofeedback (NF) as a tool to both study and treat various clinical conditions. The uses of NF are diverse, ranging across a variety of motor and sensory tasks (1-4), investigation of cortical plasticity and attention (5-9), to treatment of chronic pain, depression, and mood control (10-13).Recent advances in functional MRI (fMRI) techniques and hardware have made real-time fMRI (rtfMRI) a viable method for NF (14). This enables more anatomically specific training compared with methods such as EEG. This enhanced localization additionally allows to provide feedback to differential activation patterns (6, 15, 16), beyond simple up/down-regulation of a specific region/frequency.Another advance in the field of NF is the finding by several recent studies that participants are able to learn to successfully perform the NF paradigm, even without being given an explicit strategy (8,16). This form of implicit learning is intriguing, both because there have been reports indicating certain advantages to implicit over explicit learning (17,18), but mostly because this opens up previously unidentified pathways for therapeutic intervention, for cases for which there are no specific explicit strategies available (for instance, control over complex networks, such as in epilepsy, or over brain regions whose function is not fully elucidated).However, an important common factor in all previous NF studies was the fact that participants were aware that they were being trained, and received specific goals for this training. A fundamental question that therefore remains unanswered is whether targeted brain networks can still be modulated even in the complete absence of participants' awareness that a training process is taking place. Theories of closed-loop learning provide evidence that such implicit learning through reward cues is possible (19,20). This is an important issue, because it may open the way for NF training even in severe clinical cases such as minimally conscious or vegetative state, where such awareness is absent.In the present study, we examined this question in fMRI experiments in which participants were i...
The existence of abnormal connectivity patterns between resting state networks in neuropsychiatric disorders, including Autism Spectrum Disorder (ASD), has been well established. Traditional treatment methods in ASD are limited, and do not address the aberrant network structure. Using real-time fMRI neurofeedback, we directly trained three brain nodes in participants with ASD, in which the aberrant connectivity has been shown to correlate with symptom severity. Desired network connectivity patterns were reinforced in real-time, without participants’ awareness of the training taking place. This training regimen produced large, significant long-term changes in correlations at the network level, and whole brain analysis revealed that the greatest changes were focused on the areas being trained. These changes were not found in the control group. Moreover, changes in ASD resting state connectivity following the training were correlated to changes in behavior, suggesting that neurofeedback can be used to directly alter complex, clinically relevant network connectivity patterns.
The existence of abnormal connectivity patterns between resting state networks in neuropsychiatric disorders, including Autism Spectrum Disorder (ASD), has been well established. Traditional treatment methods in ASD are limited, and do not address the aberrant network structure. Using real-time fMRI neurofeedback, we directly trained 3 brain nodes in participants with ASD, in which the aberrant connectivity has been shown to correlate with symptom severity. 17 ASD participants and 10 control participants were scanned over multiple sessions (123 sessions in total). Desired network connectivity patterns were reinforced in realtime, without participants' awareness of the training taking place. This training regimen produced large, significant long-term changes in correlations at the network level, and whole brain analysis revealed that the greatest changes were focused on the areas being trained. These changes were not found in the control group. Moreover, changes in ASD resting state connectivity following the training were correlated to changes in behavior, suggesting that neurofeedback can be used to directly alter complex, clinically relevant network connectivity patterns. Significance StatementMany disorders are characterized by underlying abnormalities in network connectivity. These abnormalities are difficult to address with explicit training procedures (which are unlikely to target the specific abnormalities). Covert neurofeedback however, can directly target these networks, positively reinforcing the desired connections. We have developed a method for reinforcing correlations in real-time, and show that such training is effective, inducing significant, long-lasting changes in connectivity between aberrant networks in Autism SpectrumDisorder. This provides a potential mechanism for modulating aberrant correlation structures in other clinical groups as well.
One of the puzzling aspects in the visual attention literature is the discrepancy between electrophysiological and fMRI findings: whereas fMRI studies reveal strong attentional modulation in the earliest visual areas, single-unit and local field potential studies yielded mixed results. In addition, it is not clear to what extent spatial attention effects extend from early to high-order visual areas. Here we addressed these issues using electrocorticography recordings in epileptic patients. The patients performed a task that allowed simultaneous manipulation of both spatial and object-based attention. They were presented with composite stimuli, consisting of a small object (face or house) superimposed on a large one, and in separate blocks, were instructed to attend one of the objects. We found a consistent increase in broadband high-frequency (30 -90 Hz) power, but not in visual evoked potentials, associated with spatial attention starting with V1/V2 and continuing throughout the visual hierarchy. The magnitude of the attentional modulation was correlated with the spatial selectivity of each electrode and its distance from the occipital pole. Interestingly, the latency of the attentional modulation showed a significant decrease along the visual hierarchy. In addition, electrodes placed over high-order visual areas (e.g., fusiform gyrus) showed both effects of spatial and object-based attention. Overall, our results help to reconcile previous observations of discrepancy between fMRI and electrophysiology. They also imply that spatial attention effects can be found both in early and high-order visual cortical areas, in parallel with their stimulus tuning properties.
Clinical diagnosis of disorders of consciousness (DOC) caused by brain injury poses great challenges since patients are often behaviorally unresponsive. A promising new approach towards objective DOC diagnosis may be offered by the analysis of ultra-slow (<0.1 Hz) spontaneous brain activity fluctuations measured with functional magnetic resonance imaging (fMRI) during the resting-state. Previous work has shown reduced functional connectivity within the “default network”, a subset of regions known to be deactivated during engaging tasks, which correlated with the degree of consciousness impairment. However, it remains unclear whether the breakdown of connectivity is restricted to the “default network”, and to what degree changes in functional connectivity can be observed at the single subject level. Here, we analyzed resting-state inter-hemispheric connectivity in three homotopic regions of interest, which could reliably be identified based on distinct anatomical landmarks, and were part of the “Extrinsic” (externally oriented, task positive) network (pre- and postcentral gyrus, and intraparietal sulcus). Resting-state fMRI data were acquired for a group of 11 healthy subjects and 8 DOC patients. At the group level, our results indicate decreased inter-hemispheric functional connectivity in subjects with impaired awareness as compared to subjects with intact awareness. Individual connectivity scores significantly correlated with the degree of consciousness. Furthermore, a single-case statistic indicated a significant deviation from the healthy sample in 5/8 patients. Importantly, of the three patients whose connectivity indices were comparable to the healthy sample, one was diagnosed as locked-in. Taken together, our results further highlight the clinical potential of resting-state connectivity analysis and might guide the way towards a connectivity measure complementing existing DOC diagnosis.
While research of human cortical function has typically focused on task-related increases in neuronal activity, there is a growing interest in the complementary phenomenon-namely, task-induced reductions. Recent human BOLD fMRI studies have associated such reductions with a specific network termed the default mode network (DMN). However, detailed understanding of the spatiotemporal patterns of task-negative responses and particularly how they compare across different cortical networks is lacking. Here we examined this issue in a large-scale electrocorticography study in patients performing a demanding backward masking task. Our results uncovered rapid (Ͻ1 s) task-induced reductions in gamma power, often concomitant with power increase in alpha/beta bands. Importantly, these responses were found both in the DMN and sensory-motor networks. Comparing the task-negative responses across these different networks revealed similar spectral signatures and dynamics. We hypothesize that the task-negative responses may reflect a cortical switching mechanism whose role is to steer activity away from cortical networks, which are inappropriate for the task at hand.
Natural sleep provides a powerful model system for studying the neuronal correlates of awareness and state changes in the human brain. To quantitatively map the nature of sleep-induced modulations in sensory responses we presented participants with auditory stimuli possessing different levels of linguistic complexity. Ten participants were scanned using functional magnetic resonance imaging (fMRI) during the waking state and after falling asleep. Sleep staging was based on heart rate measures validated independently on 20 participants using concurrent EEG and heart rate measurements and the results were confirmed using permutation analysis. Participants were exposed to three types of auditory stimuli: scrambled sounds, meaningless word sentences and comprehensible sentences. During non-rapid eye movement (NREM) sleep, we found diminishing brain activation along the hierarchy of language processing, more pronounced in higher processing regions. Specifically, the auditory thalamus showed similar activation levels during sleep and waking states, primary auditory cortex remained activated but showed a significant reduction in auditory responses during sleep, and the high order language-related representation in inferior frontal gyrus (IFG) cortex showed a complete abolishment of responses during NREM sleep. In addition to an overall activation decrease in language processing regions in superior temporal gyrus and IFG, those areas manifested a loss of semantic selectivity during NREM sleep. Our results suggest that the decreased awareness to linguistic auditory stimuli during NREM sleep is linked to diminished activity in high order processing stations.
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