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Neural Mechanisms Determining the Duration of Task-free, Self-paced Visual Perception

Baror, Shira; Baumgarten, Thomas J; He, Biyu J
Humans spend hours each day spontaneously engaging with visual content, free from specific tasks and at their own pace. Currently, the brain mechanisms determining the duration of self-paced perceptual behavior remain largely unknown. Here, participants viewed naturalistic images under task-free settings and self-paced each image's viewing duration while undergoing EEG and pupillometry recordings. Across two independent data sets, we observed large inter- and intra-individual variability in viewing duration. However, beyond an image's presentation order and category, specific image content had no consistent effects on spontaneous viewing duration across participants. Overall, longer viewing durations were associated with sustained enhanced posterior positivity and anterior negativity in the ERPs. Individual-specific variations in the spontaneous viewing duration were consistently correlated with evoked EEG activity amplitudes and pupil size changes. By contrast, presentation order was selectively correlated with baseline alpha power and baseline pupil size. Critically, spontaneous viewing duration was strongly predicted by the temporal stability in neural activity patterns starting as early as 350 msec after image onset, suggesting that early neural stability is a key predictor for sustained perceptual engagement. Interestingly, neither bottom-up nor top-down predictions about image category influenced spontaneous viewing duration. Overall, these results suggest that individual-specific factors can influence perceptual processing at a surprisingly early time point and influence the multifaceted ebb and flow of spontaneous human perceptual behavior in naturalistic settings.
PMID: 38357932
ISSN: 1530-8898
CID: 5635852

A novel, semi-automatic procedure for generating slow change blindness stimuli

Frey, Haley G; Koenig, Lua; He, Biyu J; Brascamp, Jan W
Change blindness is the phenomenon that occurs when an observer fails to notice what would seem to be obvious changes in the features of a visual stimulus. Researchers can induce this experimentally by including visual disruptions (such as brief blanks) that coincide with the changes in question. However, change blindness can also occur in the absence of these disruptions if a change occurs sufficiently slowly. This "slow" or "gradual" change blindness phenomenon has not been extensively researched. Two plausible practical reasons for this are that there are few slow-change stimuli available, and that it is difficult to collect trial-specific responses without affecting expectations on later trials. Here, we describe a novel, semi-automatic procedure for quickly generating many slow-change stimuli. This procedure creates stimuli that have been specifically designed to allow assessment of change blindness on individual trials without influencing subsequent trials. We include the results of three validation experiments that demonstrate that these stimuli are effective and suitable for use in systematic studies of slow change blindness.
PMCID:10860497
PMID: 38348333
ISSN: 2057-2107
CID: 5635662

Next frontiers in consciousness research

He, Biyu J
Consciousness science has matured over the past three decades and is currently on the cusp of explosive growth, with the potential to transform medicine and technology. The global community recently met to synthesize the current state of knowledge and define the most exciting approaches to advance the field.
PMID: 37857090
ISSN: 1097-4199
CID: 5607662

Spatiotemporal neural dynamics of object recognition under uncertainty in humans

Wu, Yuan-Hao; Podvalny, Ella; He, Biyu J
While there is a wealth of knowledge about core object recognition-our ability to recognize clear, high-contrast object images-how the brain accomplishes object recognition tasks under increased uncertainty remains poorly understood. We investigated the spatiotemporal neural dynamics underlying object recognition under increased uncertainty by combining MEG and 7 Tesla (7T) fMRI in humans during a threshold-level object recognition task. We observed an early, parallel rise of recognition-related signals across ventral visual and frontoparietal regions that preceded the emergence of category-related information. Recognition-related signals in ventral visual regions were best explained by a two-state representational format whereby brain activity bifurcated for recognized and unrecognized images. By contrast, recognition-related signals in frontoparietal regions exhibited a reduced representational space for recognized images, yet with sharper category information. These results provide a spatiotemporally resolved view of neural activity supporting object recognition under uncertainty, revealing a pattern distinct from that underlying core object recognition.
PMID: 37184213
ISSN: 2050-084x
CID: 5541732

Towards a pluralistic neurobiological understanding of consciousness

He, Biyu J
Theories of consciousness are often based on the assumption that a single, unified neurobiological account will explain different types of conscious awareness. However, recent findings show that, even within a single modality such as conscious visual perception, the anatomical location, timing, and information flow of neural activity related to conscious awareness vary depending on both external and internal factors. This suggests that the search for generic neural correlates of consciousness may not be fruitful. I argue that consciousness science requires a more pluralistic approach and propose a new framework: joint determinant theory (JDT). This theory may be capable of accommodating different brain circuit mechanisms for conscious contents as varied as percepts, wills, memories, emotions, and thoughts, as well as their integrated experience.
PMCID:10101889
PMID: 36842851
ISSN: 1879-307x
CID: 5466632

Frequency-specific neural signatures of perceptual content and perceptual stability

Hardstone, Richard; Flounders, Matthew W; Zhu, Michael; He, Biyu J
In the natural environment, we often form stable perceptual experiences from ambiguous and fleeting sensory inputs. Which neural activity underlies the content of perception and which neural activity supports perceptual stability remains an open question. We used a bistable perception paradigm involving ambiguous images to behaviorally dissociate perceptual content from perceptual stability, and magnetoencephalography to measure whole-brain neural dynamics in humans. Combining multivariate decoding and neural state-space analyses, we found frequency-band-specific neural signatures that underlie the content of perception and promote perceptual stability, respectively. Across different types of images, non-oscillatory neural activity in the slow cortical potential (<5 Hz) range supported the content of perception. Perceptual stability was additionally influenced by the amplitude of alpha and beta oscillations. In addition, neural activity underlying perceptual memory, which supports perceptual stability when sensory input is temporally removed from view, also encodes elapsed time. Together, these results reveal distinct neural mechanisms that support the content versus stability of visual perception.
PMCID:9550226
PMID: 36125242
ISSN: 2050-084x
CID: 5351072

Neural oscillations promoting perceptual stability and perceptual memory during bistable perception

Zhu, Michael; Hardstone, Richard; He, Biyu J
Ambiguous images elicit bistable perception, wherein periods of momentary perceptual stability are interrupted by sudden perceptual switches. When intermittently presented, ambiguous images trigger a perceptual memory trace in the intervening blank periods. Understanding the neural bases of perceptual stability and perceptual memory during bistable perception may hold clues for explaining the apparent stability of visual experience in the natural world, where ambiguous and fleeting images are prevalent. Motivated by recent work showing the involvement of the right inferior frontal gyrus (rIFG) in bistable perception, we conducted a transcranial direct-current stimulation (tDCS) study with a double-blind, within-subject cross-over design to test a potential causal role of rIFG in these processes. Subjects viewed ambiguous images presented continuously or intermittently while under EEG recording. We did not find any significant tDCS effect on perceptual behavior. However, the fluctuations of oscillatory power in the alpha and beta bands predicted perceptual stability, with higher power corresponding to longer percept durations. In addition, higher alpha and beta power predicted enhanced perceptual memory during intermittent viewing. These results reveal a unified neurophysiological mechanism sustaining perceptual stability and perceptual memory when the visual system is faced with ambiguous input.
PMCID:8854562
PMID: 35177702
ISSN: 2045-2322
CID: 5163602

Long-term priors influence visual perception through recruitment of long-range feedback

Hardstone, Richard; Zhu, Michael; Flinker, Adeen; Melloni, Lucia; Devore, Sasha; Friedman, Daniel; Dugan, Patricia; Doyle, Werner K; Devinsky, Orrin; He, Biyu J
Perception results from the interplay of sensory input and prior knowledge. Despite behavioral evidence that long-term priors powerfully shape perception, the neural mechanisms underlying these interactions remain poorly understood. We obtained direct cortical recordings in neurosurgical patients as they viewed ambiguous images that elicit constant perceptual switching. We observe top-down influences from the temporal to occipital cortex, during the preferred percept that is congruent with the long-term prior. By contrast, stronger feedforward drive is observed during the non-preferred percept, consistent with a prediction error signal. A computational model based on hierarchical predictive coding and attractor networks reproduces all key experimental findings. These results suggest a pattern of large-scale information flow change underlying long-term priors' influence on perception and provide constraints on theories about long-term priors' influence on perception.
PMID: 34725348
ISSN: 2041-1723
CID: 5037932

State-related neural influences on fMRI connectivity estimation

Martin, Caroline G; He, Biyu J; Chang, Catie
The spatiotemporal structure of functional magnetic resonance imaging (fMRI) signals has provided a valuable window into the network underpinnings of human brain function and dysfunction. Although some cross-regional temporal correlation patterns (functional connectivity; FC) exhibit a high degree of stability across individuals and species, there is growing acknowledgment that measures of FC can exhibit marked changes over a range of temporal scales. Further, FC can co-vary with experimental task demands and ongoing neural processes linked to arousal, consciousness and perception, cognitive and affective state, and brain-body interactions. The increased recognition that such interrelated neural processes modulate FC measurements has raised both challenges and new opportunities in using FC to investigate brain function. Here, we review recent advances in the quantification of neural effects that shape fMRI FC and discuss the broad implications of these findings in the design and analysis of fMRI studies. We also discuss how a more complete understanding of the neural factors that shape FC measurements can resolve apparent inconsistencies in the literature and lead to more interpretable conclusions from fMRI studies.
PMID: 34560268
ISSN: 1095-9572
CID: 5026912

Spectral signature and behavioral consequence of spontaneous shifts of pupil-linked arousal in human

Podvalny, Ella; King, Leana E; He, Biyu J
Arousal levels perpetually rise and fall spontaneously. How markers of arousal - pupil size and frequency content of brain activity - relate to each other and influence behavior in humans is poorly understood. We simultaneously monitored magnetoencephalography and pupil in healthy volunteers at rest and during a visual perceptual decision-making task. Spontaneously varying pupil size correlates with power of brain activity in most frequency bands across large-scale resting-state cortical networks. Pupil size recorded at prestimulus baseline correlates with subsequent shifts in detection bias (c) and sensitivity (d'). When dissociated from pupil-linked state, prestimulus spectral power of resting state networks still predicts perceptual behavior. Fast spontaneous pupil constriction and dilation correlate with large-scale brain activity as well but not perceptual behavior. Our results illuminate the relation between central and peripheral arousal markers and their respective roles in human perceptual decision-making.
PMID: 34463255
ISSN: 2050-084x
CID: 4995772