Tobias H. Donner

Neuronal Synchronization along the Dorsal Visual Pathway Reflects the Focus of Spatial Attention

Oscillatory neuronal synchronization, within and between cortical areas, may mediate the selection of attended visual stimuli. However, it remains unclear at and between which processing stages visuospatial attention modulates oscillatory synchronization in the human brain. We thus combined magnetoencephalography (MEG) in a spatially cued motion discrimination task with source-reconstruction techniques and characterized attentional effects on neuronal synchronization across key stages of the human dorsal visual pathway. We found that visuospatial attention modulated oscillatory synchronization between visual, parietal, and prefrontal cortex in a spatially selective fashion. Furthermore, synchronized activity within these stages was selectively modulated by attention, but with markedly distinct spectral signatures and stimulus dependence between regions. Our data indicate that regionally specific oscillatory synchronization at most stages of the human dorsal visual pathway may enhance the processing of attended visual stimuli and suggest that attentional selection is mediated by frequency-specific synchronization between prefrontal, parietal, and early visual cortex.

A framework for local cortical oscillation patterns

Oscillations are a pervasive feature of neuronal activity in the cerebral cortex. Here, we propose a framework for understanding local cortical oscillation patterns in cognition: two classes of network interactions underlying two classes of cognitive functions produce different local oscillation patterns. Local excitatory-inhibitory interactions shape neuronal representations of sensory, motor and cognitive variables, and produce local gamma-band oscillations. By contrast, the linkage of such representations by integrative functions such as decision-making is mediated by long-range cortical interactions, which yield more diverse local oscillation patterns often involving the beta range. This framework reconciles different cortical oscillation patterns observed in recent studies and helps to understand the link between cortical oscillations and the fMRI signal. Our framework highlights the notion that cortical oscillations index the specific circuit-level mechanisms of cognition.

Midfrontal conflict-related theta-band power reflects neural oscillations that predict behavior

Action monitoring and conflict resolution require the rapid and flexible coordination of activity in multiple brain regions. Oscillatory neural population activity may be a key physiological mechanism underlying such rapid and flexible network coordination. EEG power modulations of theta-band (4-8 Hz) activity over the human midfrontal cortex during response conflict have been proposed to reflect neural oscillations that support conflict detection and resolution processes. However, it has remained unclear whether this frequency-band-specific activity reflects neural oscillations or nonoscillatory responses (i.e., event-related potentials). Here, we show that removing the phase-locked component of the EEG did not reduce the strength of the conflict-related modulation of the residual (i.e., non-phase-locked) theta power over midfrontal cortex. Furthermore, within-subject regression analyses revealed that the non-phase-locked theta power was a significantly better predictor of the conflict condition than was the time-domain phase-locked EEG component. Finally, non-phase-locked theta power showed robust and condition-specific (high- vs. low-conflict) cross-trial correlations with reaction time, whereas the phase-locked component did not. Taken together, our results indicate that most of the conflict-related and behaviorally relevant midfrontal EEG signal reflects a modulation of ongoing theta-band oscillations that occurs during the decision process but is not phase-locked to the stimulus or to the response.

Decision-related pupil dilation reflects upcoming choice and individual bias

Significance A number of studies reported that the pupil dilates (under constant illumination) during decision-making. Pupil dilation is also associated with the brain-wide release of modulatory neurotransmitters. It has remained unknown which specific elements of decision processes drive pupil dilation. Using a visual detection task, we here show that pupil dilation is primarily driven during, and not at the end of, a protracted decision. Further, pupil dilation differentiates between “yes” and “no” choices for conservative subjects deciding yes against their bias. Thus, pupil dilation reveals the content of the evolving decision and the decision maker’s attitude. These findings have important implications for interpreting decision-related brain activity. They also point to a possible role of neuromodulation in interacting with decision biases. A number of studies have shown that pupil size increases transiently during effortful decisions. These decision-related changes in pupil size are mediated by central neuromodulatory systems, which also influence the internal state of brain regions engaged in decision making. It has been proposed that pupil-linked neuromodulatory systems are activated by the termination of decision processes, and, consequently, that these systems primarily affect the postdecisional brain state. Here, we present pupil results that run contrary to this proposal, suggesting an important intradecisional role. We measured pupil size while subjects formed protracted decisions about the presence or absence (“yes” vs. “no”) of a visual contrast signal embedded in dynamic noise. Linear systems analysis revealed that the pupil was significantly driven by a sustained input throughout the course of the decision formation. This sustained component was larger than the transient component during the final choice (indicated by button press). The overall amplitude of pupil dilation during decision formation was bigger before yes than no choices, irrespective of the physical presence of the target signal. Remarkably, the magnitude of this pupil choice effect (yes > no) reflected the individual criterion: it was strongest in conservative subjects choosing yes against their bias. We conclude that the central neuromodulatory systems controlling pupil size are continuously engaged during decision formation in a way that reveals how the upcoming choice relates to the decision maker’s attitude. Changes in brain state seem to interact with biased decision making in the face of uncertainty.

GABA Shapes the Dynamics of Bistable Perception

Sometimes, perception fluctuates spontaneously between two distinct interpretations of a constant sensory input. These bistable perceptual phenomena provide a unique window into the neural mechanisms that create the contents of conscious perception. Models of bistable perception posit that mutual inhibition between stimulus-selective neural populations in visual cortex plays a key role in these spontaneous perceptual fluctuations. However, a direct link between neural inhibition and bistable perception has not yet been established experimentally. Here, we link perceptual dynamics in three distinct bistable visual illusions (binocular rivalry, motion-induced blindness, and structure from motion) to measurements of gamma-aminobutyric acid (GABA) concentrations in human visual cortex (as measured with magnetic resonance spectroscopy) and to pharmacological stimulation of the GABAA receptor by means of lorazepam. As predicted by a model of neural interactions underlying bistability, both higher GABA concentrations in visual cortex and lorazepam administration induced slower perceptual dynamics, as reflected in a reduced number of perceptual switches and a lengthening of percept durations. Thus, we show that GABA, the main inhibitory neurotransmitter, shapes the dynamics of bistable perception. These results pave the way for future studies into the competitive neural interactions across the visual cortical hierarchy that elicit conscious perception.

Opposite Neural Signatures of Motion-Induced Blindness in Human Dorsal and Ventral Visual Cortex

Motion-induced blindness (MIB) is a visual phenomenon in which a salient static target spontaneously fluctuates in and out of visual awareness when surrounded by a moving mask pattern. It has been hypothesized that MIB reflects an antagonistic interplay between cortical representations of the static target and moving mask. Here, we report evidence for such antagonism between human ventral and dorsal visual cortex during MIB. Functional magnetic resonance imaging (fMRI) responses in ventral visual area V4 decreased with the subjective disappearance of the target. These response decreases were specific for the cortical subregion corresponding retinotopically to the target, occurred early in time with respect to the perceptual report, and could not be explained by shifts of attention in reaction to target disappearance. At the same time, responses increased in mask-specific subregions in dorsal visual areas in and around the intraparietal sulcus. These opposite responses in ventral and dorsal visual areas occurred only during subjective target disappearance, not when the target was physically removed. Perceptual reports of target disappearance were furthermore associated with a “global” modulation of activity, which was delayed in time, and evident throughout early visual cortex, for both subjective target disappearance and physical target removal. We conclude that awareness of the target is tightly linked to the strength of its representation in ventral visual cortex, and that the mask representation in dorsal visual cortex plays a crucial role in the spontaneous suppression of the target representation during MIB.

Cortical network dynamics of perceptual decision-making in the human brain

Goal-directed behavior requires the flexible transformation of sensory evidence about our environment into motor actions. Studies of perceptual decision-making have shown that this transformation is distributed across several widely separated brain regions. Yet, little is known about how decision-making emerges from the dynamic interactions among these regions. Here, we review a series of studies, in which we characterized the cortical network interactions underlying a perceptual decision process in the human brain. We used magnetoencephalography to measure the large-scale cortical population dynamics underlying each of the sub-processes involved in this decision: the encoding of sensory evidence and action plan, the mapping between the two, and the attentional selection of task-relevant evidence. We found that these sub-processes are mediated by neuronal oscillations within specific frequency ranges. Localized gamma-band oscillations in sensory and motor cortices reflect the encoding of the sensory evidence and motor plan. Large-scale oscillations across widespread cortical networks mediate the integrative processes connecting these local networks: Gamma- and beta-band oscillations across frontal, parietal, and sensory cortices serve the selection of relevant sensory evidence and its flexible mapping onto action plans. In sum, our results suggest that perceptual decisions are mediated by oscillatory interactions within overlapping local and large-scale cortical networks.

Supersolid formation in a quantum gas breaking a continuous translational symmetry

The concept of a supersolid state combines the crystallization of a many-body system with dissipationless flow of the atoms from which it is built. This quantum phase requires the breaking of two continuous symmetries: the phase invariance of a superfluid and the continuous translational invariance to form the crystal. Despite having been proposed for helium almost 50 years ago, experimental verification of supersolidity remains elusive. A variant with only discrete translational symmetry breaking on a preimposed lattice structure—the ‘lattice supersolid’—has been realized, based on self-organization of a Bose–Einstein condensate. However, lattice supersolids do not feature the continuous ground-state degeneracy that characterizes the supersolid state as originally proposed. Here we report the realization of a supersolid with continuous translational symmetry breaking along one direction in a quantum gas. The continuous symmetry that is broken emerges from two discrete spatial symmetries by symmetrically coupling a Bose–Einstein condensate to the modes of two optical cavities. We establish the phase coherence of the supersolid and find a high ground-state degeneracy by measuring the crystal position over many realizations through the light fields that leak from the cavities. These light fields are also used to monitor the position fluctuations in real time. Our concept provides a route to creating and studying glassy many-body systems with controllably lifted ground-state degeneracies, such as supersolids in the presence of disorder.

Inter-area correlations in the ventral visual pathway reflect feature integration.

During object perception, the brain integrates simple features into representations of complex objects. A perceptual phenomenon known as visual crowding selectively interferes with this process. Here, we use crowding to characterize a neural correlate of feature integration. Cortical activity was measured with functional magnetic resonance imaging, simultaneously in multiple areas of the ventral visual pathway (V1-V4 and the visual word form area, VWFA, which responds preferentially to familiar letters), while human subjects viewed crowded and uncrowded letters. Temporal correlations between cortical areas were lower for crowded letters than for uncrowded letters, especially between V1 and VWFA. These differences in correlation were retinotopically specific, and persisted when attention was diverted from the letters. But correlation differences were not evident when we substituted the letters with grating patches that were not crowded under our stimulus conditions. We conclude that inter-area correlations reflect feature integration and are disrupted by crowding. We propose that crowding may perturb the transformations between neural representations along the ventral pathway that underlie the integration of features into objects.

Retinotopic Patterns of Correlated Fluctuations in Visual Cortex Reflect the Dynamics of Spontaneous Perceptual Suppression

While viewing certain stimuli, perception changes spontaneously in the face of constant input. For example, during “motion-induced blindness” (MIB), a small salient target spontaneously disappears and reappears when surrounded by a moving mask. Models of such bistable perceptual phenomena posit spontaneous fluctuations in neuronal activity throughout multiple stages of the visual cortical hierarchy. We used fMRI to link correlated activity fluctuations across human visual cortical areas V1 through V4 to the dynamics (rate and duration) of MIB target disappearance. We computed the correlations between the time series of fMRI activity in multiple retinotopic subregions corresponding to MIB target and mask. Linear decomposition of the matrix of temporal correlations revealed spatial patterns of activity fluctuations, regardless of whether or not these were time-locked to behavioral reports of target disappearance. The spatial pattern that dominated the activity fluctuations during MIB was spatially nonspecific, shared by all subregions, but did not reflect the dynamics of perception. By contrast, the fluctuations associated with the rate of MIB disappearance were retinotopically specific for the target subregion in V4, and the fluctuations associated with the duration of MIB disappearance states were target-specific in V1. Target-specific fluctuations in V1 have not previously been identified by averaging activity time-locked to behavioral reports of MIB disappearance. Our results suggest that different levels of the visual cortical hierarchy shape the dynamics of perception via distinct mechanisms, which are evident in distinct spatial patterns of spontaneous cortical activity fluctuations.