David J. Schwartzman

Adults Can Be Trained to Acquire Synesthetic Experiences

Synesthesia is a condition where presentation of one perceptual class consistently evokes additional experiences in different perceptual categories. Synesthesia is widely considered a congenital condition, although an alternative view is that it is underpinned by repeated exposure to combined perceptual features at key developmental stages. Here we explore the potential for repeated associative learning to shape and engender synesthetic experiences. Non-synesthetic adult participants engaged in an extensive training regime that involved adaptive memory and reading tasks, designed to reinforce 13 specific letter-color associations. Following training, subjects exhibited a range of standard behavioral and physiological markers for grapheme-color synesthesia; crucially, most also described perceiving color experiences for achromatic letters, inside and outside the lab, where such experiences are usually considered the hallmark of genuine synesthetes. Collectively our results are consistent with developmental accounts of synesthesia and illuminate a previously unsuspected potential for new learning to shape perceptual experience, even in adulthood.

A comparative study of electrical potential sensors and Ag/AgCl electrodes for characterising spontaneous and event related electroencephalagram signals

BACKGROUND Electroencephalography (EEG) is still a widely used imaging tool that combines high temporal resolution with a relatively low cost. Ag/AgCl metal electrodes have been the gold standard for non-invasively monitoring electrical brain activity. Although reliable, these electrodes have multiple drawbacks: they suffer from noise, such as offset potential drift, and usability issues, for example, difficult skin preparation and cross-coupling of adjacent electrodes. NEW METHOD In order to tackle these issues a prototype Electric Potential Sensor (EPS) device based on an auto-zero operational amplifier was developed and evaluated. The EPS is a novel active ultrahigh impedance capacitively coupled sensor. The absence of 1/f noise makes the EPS ideal for use with signal frequencies of ∼10Hz or less. A comprehensive study was undertaken to compare neural signals recorded by the EPS with a standard commercial EEG system. RESULTS Quantitatively, highly similar signals were observed between the EPS and EEG sensors for both free running and evoked brain activity with cross correlations of higher than 0.9 between the EPS and a standard benchmark EEG system. COMPARISON WITH EXISTING METHOD(S) These studies comprised measurements of both free running EEG and Event Related Potentials (ERPs) from a commercial EEG system and EPS. CONCLUSIONS The EPS provides a promising alternative with many added benefits compared to standard EEG sensors, including reduced setup time and elimination of sensor cross-coupling. In the future the scalability of the EPS will allow the implementation of a whole head ultra-dense EPS array.

Theta-burst transcranial magnetic stimulation to the prefrontal or parietal cortex does not impair metacognitive visual awareness.

Neuroimaging studies commonly associate dorsolateral prefrontal cortex (DLPFC) and posterior parietal cortex with conscious perception. However, such studies only investigate correlation, rather than causation. In addition, many studies conflate objective performance with subjective awareness. In an influential recent paper, Rounis and colleagues addressed these issues by showing that continuous theta burst transcranial magnetic stimulation (cTBS) applied to the DLPFC impaired metacognitive (subjective) awareness for a perceptual task, while objective performance was kept constant. We attempted to replicate this finding, with minor modifications, including an active cTBS control site. Using a between-subjects design for both DLPFC and posterior parietal cortices, we found no evidence of a cTBS-induced metacognitive impairment. In a second experiment, we devised a highly rigorous within-subjects cTBS design for DLPFC, but again failed to find any evidence of metacognitive impairment. One crucial difference between our results and the Rounis study is our strict exclusion of data deemed unsuitable for a signal detection theory analysis. Indeed, when we included this unstable data, a significant, though invalid, metacognitive impairment was found. These results cast doubt on previous findings relating metacognitive awareness to DLPFC, and inform the current debate concerning whether or not prefrontal regions are preferentially implicated in conscious perception.

A deep-dream virtual reality platform for studying altered perceptual phenomenology

Altered states of consciousness, such as psychotic or pharmacologically-induced hallucinations, provide a unique opportunity to examine the mechanisms underlying conscious perception. However, the phenomenological properties of these states are difficult to isolate experimentally from other, more general physiological and cognitive effects of psychoactive substances or psychopathological conditions. Thus, simulating phenomenological aspects of altered states in the absence of these other more general effects provides an important experimental tool for consciousness science and psychiatry. Here we describe such a tool, which we call the Hallucination Machine. It comprises a novel combination of two powerful technologies: deep convolutional neural networks (DCNNs) and panoramic videos of natural scenes, viewed immersively through a head-mounted display (panoramic VR). By doing this, we are able to simulate visual hallucinatory experiences in a biologically plausible and ecologically valid way. Two experiments illustrate potential applications of the Hallucination Machine. First, we show that the system induces visual phenomenology qualitatively similar to classical psychedelics. In a second experiment, we find that simulated hallucinations do not evoke the temporal distortion commonly associated with altered states. Overall, the Hallucination Machine offers a valuable new technique for simulating altered phenomenology without directly altering the underlying neurophysiology.

Coordinated neural, behavioral, and phenomenological changes in perceptual plasticity through overtraining of synesthetic associations

ABSTRACT Synesthesia is associated with additional perceptual experiences, which are automatically and consistently triggered by specific inducing stimuli. Synesthesia is also accompanied by more general sensory and cortical changes, including enhanced modality‐specific cortical excitability. Extensive cognitive training has been shown to generate synesthesia‐like phenomenology but whether these experiences are accompanied by neurophysiological changes characteristic of synesthesia remains unknown. Addressing this question provides a unique opportunity to elucidate the neural basis of perceptual plasticity relevant to conscious experiences. Here we investigate whether extensive training of letter‐color associations leads not only to synesthetic experiences, but also to changes in cortical excitability. We confirm that overtraining synesthetic associations results in synesthetic phenomenology. Stroop tasks further reveal synesthesia‐like performance following training. Electroencephalography and transcranial magnetic stimulation show, respectively, enhanced visual evoked potentials (in response to untrained patterns) and lower phosphene thresholds, demonstrating specific cortical changes. An active (using letter‐symbol training) and a passive control confirmed these results were due to letter‐color training and not simply to repeated testing. Summarizing, we demonstrate specific cortical changes, following training‐induced acquisition of synesthetic phenomenology that are characteristic of genuine synesthesia. Collectively, our data reveal dramatic plasticity in human visual perception, expressed through a coordinated set of behavioral, neurophysiological, and phenomenological changes. HIGHLIGHTSProlonged synesthetic associations training results in synesthetic phenomenology.Trained synesthetic phenomenology is associated with perceptual differences in visual areas.Trained synesthetic phenomenology is associated with behavioral synesthetic markers.Prolonged association training does not generally lead to similar cortical changes.Collectively, the data reveal dramatic plasticity in human visual perception.

The Hallucination Machine: A Deep-Dream VR platform for Studying the Phenomenology of Visual Hallucinations

Altered states of consciousness, such as psychotic or pharmacologically-induced hallucinations, provide a unique opportunity to examine the mechanisms underlying conscious perception. However, the phenomenological properties of these states are difficult to isolate experimentally from other, more general physiological and cognitive effects of psychoactive substances or psychopathological conditions. Thus, simulating phenomenological aspects of altered states in the absence of these other more general effects provides an important experimental tool for consciousness science and psychiatry. Here we describe such a tool, the Hallucination Machine. It comprises a novel combination of two powerful technologies: deep convolutional neural networks (DCNNs) and panoramic videos of natural scenes, viewed immersively through a head-mounted display (panoramic VR). By doing this, we are able to simulate visual hallucinatory experiences in a biologically plausible and ecologically valid way. Two experiments illustrate potential applications of the Hallucination Machine. First, we show that the system induces visual phenomenology qualitatively similar to classical psychedelics. In a second experiment, we find that simulated hallucinations do not evoke the temporal distortion commonly associated with altered states. Overall, the Hallucination Machine offers a valuable new technique for simulating altered phenomenology without directly altering the underlying neurophysiology.

Visual Perceptual Echo Reflects Learning of Regularities in Rapid Luminance Sequences

A novel neural signature of active visual processing has recently been described in the form of the “perceptual echo”, in which the cross-correlation between a sequence of randomly fluctuating luminance values and occipital electrophysiological signals exhibits a long-lasting periodic (∼100 ms cycle) reverberation of the input stimulus (VanRullen and Macdonald, 2012). As yet, however, the mechanisms underlying the perceptual echo and its function remain unknown. Reasoning that natural visual signals often contain temporally predictable, though nonperiodic features, we hypothesized that the perceptual echo may reflect a periodic process associated with regularity learning. To test this hypothesis, we presented subjects with successive repetitions of a rapid nonperiodic luminance sequence, and examined the effects on the perceptual echo, finding that echo amplitude linearly increased with the number of presentations of a given luminance sequence. These data suggest that the perceptual echo reflects a neural signature of regularity learning. Furthermore, when a set of repeated sequences was followed by a sequence with inverted luminance polarities, the echo amplitude decreased to the same level evoked by a novel stimulus sequence. Crucially, when the original stimulus sequence was re-presented, the echo amplitude returned to a level consistent with the number of presentations of this sequence, indicating that the visual system retained sequence-specific information, for many seconds, even in the presence of intervening visual input. Altogether, our results reveal a previously undiscovered regularity learning mechanism within the human visual system, reflected by the perceptual echo. SIGNIFICANCE STATEMENT How the brain encodes and learns fast-changing but nonperiodic visual input remains unknown, even though such visual input characterizes natural scenes. We investigated whether the phenomenon of “perceptual echo” might index such learning. The perceptual echo is a long-lasting reverberation between a rapidly changing visual input and evoked neural activity, apparent in cross-correlations between occipital EEG and stimulus sequences, peaking in the alpha (∼10 Hz) range. We indeed found that perceptual echo is enhanced by repeatedly presenting the same visual sequence, indicating that the human visual system can rapidly and automatically learn regularities embedded within fast-changing dynamic sequences. These results point to a previously undiscovered regularity learning mechanism, operating at a rate defined by the alpha frequency.

Neurite orientation and dispersion density imaging (NODDI) detects cortical and corticospinal tract degeneration in ALS

Background Corticospinal tract (CST) degeneration and cortical atrophy are consistent features of amyotrophic lateral sclerosis (ALS). We hypothesised that neurite orientation dispersion and density imaging (NODDI), a multicompartment model of diffusion MRI, would reveal microstructural changes associated with ALS within the CST and precentral gyrus (PCG) ‘in vivo’. Methods 23 participants with sporadic ALS and 23 healthy controls underwent diffusion MRI. Neurite density index (NDI), orientation dispersion index (ODI) and free water fraction (isotropic compartment (ISO)) were derived. Whole brain voxel-wise analysis was performed to assess for group differences. Standard diffusion tensor imaging (DTI) parameters were computed for comparison. Subgroup analysis was performed to investigate for NODDI parameter differences relating to bulbar involvement. Correlation of NODDI parameters with clinical variables were also explored. The results were accepted as significant where p<0.05 after family-wise error correction at the cluster level, clusters formed with p<0.001. Results In the ALS group NDI was reduced in the extensive regions of the CST, the corpus callosum and the right PCG. ODI was reduced in the right anterior internal capsule and the right PCG. Significant differences in NDI were detected between subgroups stratified according to the presence or absence of bulbar involvement. ODI and ISO correlated with disease duration. Conclusions NODDI demonstrates that axonal loss within the CST is a core feature of degeneration in ALS. This is the main factor contributing to the altered diffusivity profile detected using DTI. NODDI also identified dendritic alterations within the PCG, suggesting microstructural cortical dendritic changes occur together with CST axonal damage.

Response to Ruby et al: on a ‘failed’ attempt to manipulate conscious perception with transcranial magnetic stimulation to prefrontal cortex

Does disruption of prefrontal cortical activity using transcranial magnetic stimulation (TMS) impair visual metacognition? An initial study supporting this idea (Rounis, Maniscalco, Rothwell, Passingham, & Lau, 2010) motivated an attempted replication and extension (Bor, Schwartzman, Barrett, & Seth, 2017). Bor et al. failed to replicate the initial study, concluding that there was not good evidence that TMS to dorsolateral prefrontal cortex impairs visual metacognition. This failed replication has recently been critiqued by some of the authors of the initial study (Ruby, Maniscalco, & Peters, 2018). Here we argue that these criticisms are misplaced. In our response, we encounter some more general issues concerning good practice in replication of cognitive neuroscience studies, and in setting criteria for excluding data when employing statistical analyses like signal detection theory. We look forward to further studies investigating the role of prefrontal cortex in metacognition, with increasingly refined methodologies, motivated by the discussions in this series of papers.

Fractionation of parietal function in bistable perception probed with concurrent TMS-EEG

When visual input has conflicting interpretations, conscious perception can alternate spontaneously between these possible interpretations. This is called bistable perception. Previous neuroimaging studies have indicated the involvement of two right parietal areas in resolving perceptual ambiguity (ant-SPLr and post-SPLr). Transcranial magnetic stimulation (TMS) studies that selectively interfered with the normal function of these regions suggest that they play opposing roles in this type of perceptual switch. In the present study, we investigated this fractionation of parietal function by use of combined TMS with electroencephalography (EEG). Specifically, while participants viewed either a bistable stimulus, a replay stimulus, or resting-state fixation, we applied single pulse TMS to either location independently while simultaneously recording EEG. Combined with participant’s individual structural magnetic resonance imaging (MRI) scans, this dataset allows for complex analyses of the effect of TMS on neural time series data, which may further elucidate the causal role of the parietal cortex in ambiguous perception.