Papers by Naotsugu Tsuchiya
eNeuro, 2017
A significant problem in neuroscience concerns the distinction between neural processing that is ... more A significant problem in neuroscience concerns the distinction between neural processing that is correlated with conscious percepts from processing that is not. Here, we tested if a hierarchical structure of causal interactions between neuronal populations correlates with conscious perception. We derived the hierarchical causal structure as a pattern of integrated information, inspired by the integrated information theory of consciousness. We computed integrated information patterns from intracranial electrocorticography from 6 human neurosurgical patients with electrodes implanted over lateral and ventral cortices. During recording, subjects viewed continuous flash suppression and backward masking stimuli intended to dissociate conscious percept from stimulus, and unmasked suprathreshold stimuli. Object-sensitive areas revealed correspondence between conscious percepts and integrated information patterns. We quantified this correspondence using unsupervised classification methods that revealed clustering of visual experiences with integrated information, but not with broader information measures including mutual information and entropy. Our findings point to a significant role of locally integrated information for understanding the neural substrate of conscious object perception.
Illusions that produce perceptual suppression despite constant retinal input are used to manipula... more Illusions that produce perceptual suppression despite constant retinal input are used to manipulate visual consciousness. Here we report on a powerful variant of existing techniques, continuous flash suppression. Distinct images flashed successively at ~10 Hz into one eye reliably suppress an image presented to the other eye. The duration of perceptual suppression is at least ten times greater than that produced by binocular rivalry. Using this tool we show that the strength of the negative afterimage of an adaptor was reduced by half when it was perceptually suppressed by input from the other eye. The more completely the adaptor was suppressed, the more strongly the afterimage intensity was reduced. Paradoxically, trial-to-trial visibility of the adaptor did not correlate with the degree of reduction. Our results imply that formation of afterimages involves neuronal structures that access input from both eyes but that do not correspond directly to the neuronal correlates of perceptual awareness. The question of the neuronal correlates of conscious perception has seen renewed interest over the last decade 1. One powerful tool in this area is illusions that give rise to effects that are measurable, yet are not, or are only occasionally, consciously seen 2–5. In backward masking 6 , inattentional blindness 7 , motion-induced blindness 8 , binocular rivalry 9–16 and flash suppression 11,17–19 , an image is presented to one or both eyes of the observer yet is not seen. Binocular rivalry is a popular method to determine if a visual aftereffect occurs before or after the neuronal site for the suppression of rivalry 2,20–23. In binocular rivalry, two different images are shown to the two eyes, and the subject's percept alternates between one and the other image 24. The strength of the aftereffect when the adaptor is presented to one eye and is plainly visible throughout the adaptation period is compared with the aftereffect when the adaptor is suppressed by the input to the other eye. However, the duration and timing of perceptual suppression are difficult to control because of the stochastic nature of rivalry. Flash suppression 11,17–19 provides better control over the timing of suppression , but at the price of shorter periods of suppression, too brief to produce strong aftereffects. Furthermore, flash suppression requires a pre-adapting period, preventing complete unawareness of the adaptor. Here we combine aspects of both binocular rivalry and flash suppression into a potent procedure we term continuous flash suppression (CFS). We continuously flash different images rapidly into one eye while the input to the corresponding location in the other eye remains the same (see demonstration at http://www.klab.caltech.edu/~naotsu/ CFSdemo.html). Most observers do not see the image in one eye even though it is present for a long time, sometimes for several minutes. We used CFS to examine the neuronal site for negative afterimages. These are vivid percepts that demonstrate the tenuous link between physical stimuli and their associated subjective percepts. A variety of evidence supports their origin among neurons in the retina 25–31 or lateral geniculate nucleus (LGN) 32. In particular, negative afterimages do not transfer across eyes, nor is their strength reduced by suppression of the inducing image by pressure blinding 20,33 (but see ref. 29). Neither binocular rivalry 20 nor motion-induced blindness (MIB) 5 reduces either the duration or the strength of afterimages. All of these observations suggest that afterimages are retinal phenomena. However, both binocular rivalry and MIB suppress the adaptor only intermittently. By using CFS, we asked what happens when the adapting stimulus is completely suppressed from awareness. We found that when an adaptor was reliably suppressed by CFS, the intensity of the negative afterimage of the adaptor was reduced by half. Our results imply that formation of afterimages involves neuronal structures that access input from both eyes but that do not correspond directly to the neuronal correlates of perceptual awareness. RESULTS Prolonged invisibility by continuous flash suppression We first compared the initial duration of stimulus suppression in CFS and binocular rivalry without pre-exposure to the suppressed image. While a constant, gray image was presented to one eye, CFS stimuli composed of different Mondrians were presented at the corresponding location in the other eye (Fig. 1). Each Mondrian was replaced by a different pattern every 100 ms. Seventeen naive subjects pressed a button as soon as any part of the gray figure became visible. The mean initial suppression time in 16 trials was 4.3 s for binocular rivalry and 56.0 s for CFS (13 times longer than for binocular rivalry; paired t-test, t-score ¼ 4.81, d.f. ¼ 16, P o 0.001). In 40 out of 272 CFS trials, no part of the gray image was seen at all for the full 3-min trial. As we treated those
When searching a crowd, people can detect a target face only by direct fixation and attention. On... more When searching a crowd, people can detect a target face only by direct fixation and attention. Once the target is found, it is consciously experienced and remembered, but what is the perceptual fate of the fixated nontarget faces? Whereas introspection suggests that one may remember nontargets, previous studies have proposed that almost no memory should be retained. Using a gaze-contingent paradigm, we asked subjects to visually search for a target face within a crowded natural scene and then tested their memory for nontarget faces, as well as their confidence in those memories. Subjects remembered up to seven fixated, nontarget faces with more than 70% accuracy. Memory accuracy was correlated with trial-by-trial confidence ratings, which implies that the memory was consciously maintained and accessed. When the search scene was inverted, no more than three nontarget faces were remembered. These findings imply that incidental memory for faces, such as those recalled by eyewitnesses, is more reliable than is usually assumed.
Neuropsychologia, Jan 31, 2017
Manipulation of multisensory integration induces illusory perceptions of body ownership. Patients... more Manipulation of multisensory integration induces illusory perceptions of body ownership. Patients with Parkinson's disease (PD), a neurodegenerative disorder characterised by striatal dopamine deficiency, are prone to illusions and hallucinations and have sensory deficits. Dopaminergic treatment also aggravates hallucinations in PD. Whether multisensory integration in body ownership is altered by PD is unexplored. To study the effect of dopamine neurotransmission on illusory perceptions of body ownership. We studied the Rubber Hand Illusion (RHI) in 21 PD patients (on- and off-medication) and 21 controls. In this experimental paradigm, synchronous stroking of a rubber hand and the subject's hidden real hand results in the illusory experience of 'feeling' the rubber hand, and proprioceptive mislocalisation of the real hand towards the rubber hand ('proprioceptive drift'). Asynchronous stroking typically attenuates the RHI. The effect of PD on illusory experien...
What characteristics of neural activity distinguish the awake and anesthetized brain? Drugs such ... more What characteristics of neural activity distinguish the awake and anesthetized brain? Drugs such as isoflurane abolish behavioral responsiveness in all animals, implying evolutionarily conserved mechanisms. However, it is unclear whether this conservation is reflected at the level of neural activity. Studies in humans have shown that anesthesia is characterized by spatially distinct spectral and coherence signatures that have also been implicated in the global impairment of cortical communication. We questioned whether anesthesia has similar effects on global and local neural processing in one of the smallest brains, that of the fruit fly (Drosophila melanogaster). Using a recently developed multielectrode technique, we recorded local field potentials from different areas of the fly brain simultaneously, while manipulating the concentration of isoflurane. Flickering visual stimuli ('frequency tags') allowed us to track evoked responses in the frequency domain and measure the effects of isoflurane throughout the brain. We found that isoflurane reduced power and coherence at the tagging frequency (13 or 17 Hz) in central brain regions. Unexpectedly, isoflurane increased power and coherence at twice the tag frequency (26 or 34 Hz) in the optic lobes of the fly, but only for specific stimulus configurations. By modeling the periodic responses, we show that the increase in power in peripheral areas can be attributed to local neuroanatomy. We further show that the effects on coherence can be explained by impacted signal-to-noise ratios. Together, our results show that general anesthesia has distinct local and global effects on neuronal processing in the fruit fly brain.
NeuroImage, 2016
Electrocorticography (ECoG) constitutes a powerful and promising neural recording modality in hum... more Electrocorticography (ECoG) constitutes a powerful and promising neural recording modality in humans and animals. ECoG signals are often decomposed into several frequency bands, among which the so-called high-gamma band (80-250Hz) has been proposed to reflect local cortical functions near the cortical surface below the ECoG electrodes. It is typically assumed that the lower the frequency bands, the lower the spatial resolution of the signals; thus, there is not much to gain by analyzing the event-related changes of the ECoG signals in the lower-frequency bands. However, differences across frequency bands have not been systematically investigated. To address this issue, we recorded ECoG activity from two awake monkeys performing a retinotopic mapping task. We characterized the spatiotemporal profiles of the visual responses in the time-frequency domain. We defined the preferred spatial position, receptive field (RF), and response latencies of band-limited power (BLP) (i.e., alpha [3....
PloS one, 2015
Primate visual systems process natural images in a hierarchical manner: at the early stage, neuro... more Primate visual systems process natural images in a hierarchical manner: at the early stage, neurons are tuned to local image features, while neurons in high-level areas are tuned to abstract object categories. Standard models of visual processing assume that the transition of tuning from image features to object categories emerges gradually along the visual hierarchy. Direct tests of such models remain difficult due to confounding alteration in low-level image properties when contrasting distinct object categories. When such contrast is performed in a classic functional localizer method, the desired activation in high-level visual areas is typically accompanied with activation in early visual areas. Here we used a novel image-modulation method called SWIFT (semantic wavelet-induced frequency-tagging), a variant of frequency-tagging techniques. Natural images modulated by SWIFT reveal object semantics periodically while keeping low-level properties constant. Using functional magnetic...
PLOS Computational Biology, 2016
Accumulating evidence indicates that the capacity to integrate information in the brain is a prer... more Accumulating evidence indicates that the capacity to integrate information in the brain is a prerequisite for consciousness. Integrated Information Theory (IIT) of consciousness provides a mathematical approach to quantifying the information integrated in a system, called integrated information, Φ. Integrated information is defined theoretically as the amount of information a system generates as a whole, above and beyond the amount of information its parts independently generate. IIT predicts that the amount of integrated information in the brain should reflect levels of consciousness. Empirical evaluation of this theory requires computing integrated information from neural data acquired from experiments, although difficulties with using the original measure Φ precludes such computations. Although some practical measures have been previously proposed, we found that these measures fail to satisfy the theoretical requirements as a measure of integrated information. Measures of integrated information should satisfy the lower and upper bounds as follows: The lower bound of integrated information should be 0 and is equal to 0 when the system does not generate information (no information) or when the system comprises independent parts (no integration). The upper bound of integrated information is the amount of information generated by the whole system. Here we derive the novel practical measure Φ* by introducing a concept of mismatched decoding developed from information theory. We show that Φ* is properly bounded from below and above, as required, as a measure of integrated information. We derive the analytical expression of Φ* under the Gaussian assumption, which makes it readily applicable to experimental data. Our novel measure Φ* can generally be used as a measure of integrated information in research on consciousness, and also as a tool for network analysis on diverse areas of biology.
Trends in Cognitive Sciences, 2008
Advances in Consciousness Research, 2015
Trends in cognitive sciences, 2015
The goal of consciousness research is to reveal the neural basis of phenomenal experience. To stu... more The goal of consciousness research is to reveal the neural basis of phenomenal experience. To study phenomenology, experimenters seem obliged to ask reports from the subjects to ascertain what they experience. However, we argue that the requirement of reports has biased the search for the neural correlates of consciousness over the past decades. More recent studies attempt to dissociate neural activity that gives rise to consciousness from the activity that enables the report; in particular, no-report paradigms have been utilized to study conscious experience in the full absence of any report. We discuss the advantages and disadvantages of report-based and no-report paradigms, and ask how these jointly bring us closer to understanding the true neural basis of consciousness.
Background: Among the most prominent features of the social communication impairment in autism is... more Background: Among the most prominent features of the social communication impairment in autism is the tendency to avoid direct eye contact with others. From a young age, children with autism look at faces less than typically developing children and tend to avoid eye contact, even with their primary caregiver. However, there is controversy over the reason for this reduced eye contact. Do they avoid eye contact because they experience the eyes of others to be aversive? Or, are they not motivated to look at eyes because they find the eyes uninteresting? Objectives: To investigate the underlying causes for this reduced eye contact and abnormal facial fixation behavior, we monitored gaze fixation and pupillary diameter as a measure of autonomic response in children with autism and age-matched typically developing children while they looked at human emotional faces. Methods: A group of high-functioning individuals with autism (n=20) was compared to a group of typically developing children...
DESCRIPTION Measuring integrated information from the decoding perspective
Frontiers in Human Neuroscience, 2012
Uploads
Papers by Naotsugu Tsuchiya