Dynamic divisive normalization circuits explain and predict change detection in monkey area MT.

Sudden changes in visual scenes often indicate important events for behavior. For their quick and reliable detection, the brain must be capable to process these changes as independently as possible from its current activation state. In motion-selective area MT, neurons respond to instantaneous speed changes with pronounced transients, often far exceeding the expected response as derived from their speed tuning profile. We here show that this complex, non-linear behavior emerges from the combined temporal dynamics of excitation and divisive inhibition, and provide a comprehensive mathematical analysis. A central prediction derived from this investigation is that attention increases the steepness of the transient response irrespective of the activation state prior to a stimulus change, and irrespective of the sign of the change (i.e. irrespective of whether the stimulus is accelerating or decelerating). Extracellular recordings of attention-dependent representation of both speed increments and decrements confirmed this prediction and suggest that improved change detection derives from basic computations in a canonical cortical circuitry.

Visual Stimulus Content in V4 Is Conveyed by Gamma-Rhythmic Information Packages.

Selective visual attention allows the brain to focus on behaviorally relevant information while ignoring irrelevant signals. As a possible mechanism, routing-by-synchronization was proposed: neural populations receiving attended signals align their gamma-rhythmic activity to that of the sending populations, such that incoming spikes arrive at excitability peaks of receiving populations, enhancing signal transfer. Conversely, non-attended signals arrive unaligned to the receiver's oscillation, reducing signal transfer. Therefore, visual signals should be transferred through gamma-rhythmic bursts of information, resulting in a modulation of the stimulus content within the receiving population's activity by its gamma phase and amplitude. To test this prediction, we quantified gamma-phase-dependent stimulus content within neural activity from area V4 of two male macaques performing a visual attention task. For the attended stimulus, we find highest stimulus information content near excitability peaks, an effect that increases with oscillation amplitude, establishing a functional link between selective processing and gamma-activity.SIGNIFICANCE STATEMENT The ability to focus on the behaviorally relevant signals is essential for the brain to cope with the continuous, high-dimensional stream of sensory information it receives. What are the neural mechanisms which allow such selective processing in the visual system? We analyzed data from area V4 and found that the amount of visual signal information content is tightly linked to the phase of local gamma-rhythmic activity, with maximal signal content occurring near peaks of neural excitability. Our investigations provide direct evidence that selective attention relies on rhythmic temporal coordination between visual areas, and establish novel methods for pinpointing pulsed transmission schemes in neural data.

Causally Investigating Cortical Dynamics and Signal Processing by Targeting Natural System Attractors With Precisely Timed (Electrical) Stimulation.

Electrical stimulation is a promising tool for interacting with neuronal dynamics to identify neural mechanisms that underlie cognitive function. Since effects of a single short stimulation pulse typically vary greatly and depend on the current network state, many experimental paradigms have rather resorted to continuous or periodic stimulation in order to establish and maintain a desired effect. However, such an approach explicitly leads to forced and "unnatural" brain activity. Further, continuous stimulation can make it hard to parse the recorded activity and separate neural signal from stimulation artifacts. In this study we propose an alternate strategy: by monitoring a system in realtime, we use the existing preferred states or attractors of the network and apply short and precise pulses in order to switch between those states. When pushed into one of its attractors, one can use the natural tendency of the system to remain in such a state to prolong the effect of a stimulation pulse, opening a larger window of opportunity to observe the consequences on cognitive processing. To elaborate on this idea, we consider flexible information routing in the visual cortex as a prototypical example. When processing a stimulus, neural populations in the visual cortex have been found to engage in synchronized gamma activity. In this context, selective signal routing is achieved by changing the relative phase between oscillatory activity in sending and receiving populations (communication through coherence, CTC). In order to explore how perturbations interact with CTC, we investigate a network of interneuronal gamma (ING) oscillators composed of integrate-and-fire neurons exhibiting similar synchronization and signal routing phenomena. We develop a closed-loop stimulation paradigm based on the phase-response characteristics of the network and demonstrate its ability to establish desired synchronization states. By measuring information content throughout the model, we evaluate the effect of signal contamination caused by the stimulation in relation to the magnitude of the injected pulses and intrinsic noise in the system. Finally, we demonstrate that, up to a critical noise level, precisely timed perturbations can be used to artificially induce the effect of attention by selectively routing visual signals to higher cortical areas.

Contour Integration in Dynamic Scenes: Impaired Detection Performance in Extended Presentations.

Since scenes in nature are highly dynamic, perception requires an on-going and robust integration of local information into global representations. In vision, contour integration (CI) is one of these tasks, and it is performed by our brain in a seemingly effortless manner. Following the rule of good continuation, oriented line segments are linked into contour percepts, thus supporting important visual computations such as the detection of object boundaries. This process has been studied almost exclusively using static stimuli, raising the question of whether the observed robustness and "pop-out" quality of CI carries over to dynamic scenes. We investigate contour detection in dynamic stimuli where targets appear at random times by Gabor elements aligning themselves to form contours. In briefly presented displays (230 ms), a situation comparable to classical paradigms in CI, performance is about 87%. Surprisingly, we find that detection performance decreases to 67% in extended presentations (about 1.9-3.8 s) for the same target stimuli. In order to observe the same reduction with briefly presented stimuli, presentation time has to be drastically decreased to intervals as short as 50 ms. Cueing a specific contour position or shape helps in partially compensating this deterioration, and only in extended presentations combining a location and a shape cue was more efficient than providing a single cue. Our findings challenge the notion of CI as a mainly stimulus-driven process leading to pop-out percepts, indicating that top-down processes play a much larger role in supporting fundamental integration processes in dynamic scenes than previously thought.

Contextual Interactions in Grating Plaid Configurations Are Explained by Natural Image Statistics and Neural Modeling.

Processing natural scenes requires the visual system to integrate local features into global object descriptions. To achieve coherent representations, the human brain uses statistical dependencies to guide weighting of local feature conjunctions. Pairwise interactions among feature detectors in early visual areas may form the early substrate of these local feature bindings. To investigate local interaction structures in visual cortex, we combined psychophysical experiments with computational modeling and natural scene analysis. We first measured contrast thresholds for 2 × 2 grating patch arrangements (plaids), which differed in spatial frequency composition (low, high, or mixed), number of grating patch co-alignments (0, 1, or 2), and inter-patch distances (1° and 2° of visual angle). Contrast thresholds for the different configurations were compared to the prediction of probability summation (PS) among detector families tuned to the four retinal positions. For 1° distance the thresholds for all configurations were larger than predicted by PS, indicating inhibitory interactions. For 2° distance, thresholds were significantly lower compared to PS when the plaids were homogeneous in spatial frequency and orientation, but not when spatial frequencies were mixed or there was at least one misalignment. Next, we constructed a neural population model with horizontal laminar structure, which reproduced the detection thresholds after adaptation of connection weights. Consistent with prior work, contextual interactions were medium-range inhibition and long-range, orientation-specific excitation. However, inclusion of orientation-specific, inhibitory interactions between populations with different spatial frequency preferences were crucial for explaining detection thresholds. Finally, for all plaid configurations we computed their likelihood of occurrence in natural images. The likelihoods turned out to be inversely related to the detection thresholds obtained at larger inter-patch distances. However, likelihoods were almost independent of inter-patch distance, implying that natural image statistics could not explain the crowding-like results at short distances. This failure of natural image statistics to resolve the patch distance modulation of plaid visibility remains a challenge to the approach.

The role of eye movements in a contour detection task.

Vision combines local feature integration with active viewing processes, such as eye movements, to perceive complex visual scenes. However, it is still unclear how these processes interact and support each other. Here, we investigated how the dynamics of saccadic eye movements interact with contour integration, focusing on situations in which contours are difficult to find or even absent. We recorded observers' eye movements while they searched for a contour embedded in a background of randomly oriented elements. Task difficulty was manipulated by varying the contour's path angle. An association field model of contour integration was employed to predict potential saccade targets by identifying stimulus locations with high contour salience. We found that the number and duration of fixations increased with the increasing path angle of the contour. In addition, fixation duration increased over the course of a trial, and the time course of saccade amplitude depended on the percept of observers. Model fitting revealed that saccades fully compensate for the reduced saliency of peripheral contour targets. Importantly, our model predicted fixation locations to a considerable degree, indicating that observers fixated collinear elements. These results show that contour integration actively guides eye movements and determines their spatial and temporal parameters.

Toward high performance, weakly invasive brain computer interfaces using selective visual attention.

Brain-computer interfaces have been proposed as a solution for paralyzed persons to communicate and interact with their environment. However, the neural signals used for controlling such prostheses are often noisy and unreliable, resulting in a low performance of real-world applications. Here we propose neural signatures of selective visual attention in epidural recordings as a fast, reliable, and high-performance control signal for brain prostheses. We recorded epidural field potentials with chronically implanted electrode arrays from two macaque monkeys engaged in a shape-tracking task. For single trials, we classified the direction of attention to one of two visual stimuli based on spectral amplitude, coherence, and phase difference in time windows fixed relative to stimulus onset. Classification performances reached up to 99.9%, and the information about attentional states could be transferred at rates exceeding 580 bits/min. Good classification can already be achieved in time windows as short as 200 ms. The classification performance changed dynamically over the trial and modulated with the task's varying demands for attention. For all three signal features, the information about the direction of attention was contained in the γ-band. The most informative feature was spectral amplitude. Together, these findings establish a novel paradigm for constructing brain prostheses as, for example, virtual spelling boards, promising a major gain in performance and robustness for human brain-computer interfaces.

Optimality of human contour integration.

For processing and segmenting visual scenes, the brain is required to combine a multitude of features and sensory channels. It is neither known if these complex tasks involve optimal integration of information, nor according to which objectives computations might be performed. Here, we investigate if optimal inference can explain contour integration in human subjects. We performed experiments where observers detected contours of curvilinearly aligned edge configurations embedded into randomly oriented distractors. The key feature of our framework is to use a generative process for creating the contours, for which it is possible to derive a class of ideal detection models. This allowed us to compare human detection for contours with different statistical properties to the corresponding ideal detection models for the same stimuli. We then subjected the detection models to realistic constraints and required them to reproduce human decisions for every stimulus as well as possible. By independently varying the four model parameters, we identify a single detection model which quantitatively captures all correlations of human decision behaviour for more than 2000 stimuli from 42 contour ensembles with greatly varying statistical properties. This model reveals specific interactions between edges closely matching independent findings from physiology and psychophysics. These interactions imply a statistics of contours for which edge stimuli are indeed optimally integrated by the visual system, with the objective of inferring the presence of contours in cluttered scenes. The recurrent algorithm of our model makes testable predictions about the temporal dynamics of neuronal populations engaged in contour integration, and it suggests a strong directionality of the underlying functional anatomy.

Perceptual inference predicts contextual modulations of sensory responses.

Sensory receptive fields (RFs) vary as a function of stimulus properties and measurement methods. Previous stimuli or surrounding stimuli facilitate, suppress, or change the selectivity of sensory neurons' responses. Here, we propose that these spatiotemporal contextual dependencies are signatures of efficient perceptual inference and can be explained by a single neural mechanism, input targeted divisive inhibition. To respond both selectively and reliably, sensory neurons should behave as active predictors rather than passive filters. In particular, they should remove input they can predict ("explain away") from the synaptic inputs to all other neurons. This implies that RFs are constantly and dynamically reshaped by the spatial and temporal context, while the true selectivity of sensory neurons resides in their "predictive field." This approach motivates a reinvestigation of sensory representations and particularly the role and specificity of surround suppression and adaptation in sensory areas.

Attention improves object representation in visual cortical field potentials.

Selective attention improves perception and modulates neuronal responses, but how attention-dependent changes of cortical activity improve the processing of attended objects is an open question. Changes in total signal strength or enhancements in signal-to-noise ratio have been proposed as putative mechanisms. However, it is still not clear whether, and to what extent, these processes contribute to the large perceptual improvements. We studied the ability to discriminate states of activity in visual cortex evoked by differently shaped objects depending on selective attention in monkeys. We found that gamma-band activity from V4 and V1 contains a high amount of information about stimulus shape, which increases for V4 recordings considerably with attention in successful trials, but not in case of behavioral errors. This effect resulted from enhanced differences between the stimulus-specific distributions of power spectral amplitudes. It could be explained neither by enhancements of signal-to-noise ratios, nor by changes in total signal power. Instead our results indicate that attention causes underlying cortical network states to become more distinct for different stimuli, providing a new neurophysiological explanation for improvements of behavioral performance by attention. The absence of the enhancement in discriminability in trials with behavioral errors demonstrates the relevance of this novel neural mechanism for perception.

Towards on-line adaptation of neuro-prostheses with neuronal evaluation signals.

Many experiments have successfully demonstrated that prosthetic devices for restoring lost body functions can in principle be controlled by brain signals. However, stable long-term application of these devices, required for paralyzed patients, may suffer substantially from on-going signal changes for example adapting neural activities or movements of the electrodes recording brain activity. These changes currently require tedious re-learning procedures which are conducted and supervised under laboratory conditions, hampering the everyday use of such devices. As an efficient alternative to current methods we here propose an on-line adaptation scheme that exploits a hypothetical secondary signal source from brain regions reflecting the user's affective evaluation of the current neuro- prosthetic's performance. For demonstrating the feasibility of our idea, we simulate a typical prosthetic setup controlling a virtual robotic arm. Hereby we use the additional, hypothetical evaluation signal to adapt the decoding of the intended arm movement which is subjected to large non-stationarities. Even with weak signals and high noise levels typically encountered in recording brain activities, our simulations show that prosthetic devices can be adapted successfully during everyday usage, requiring no special training procedures. Furthermore, the adaptation is shown to be stable against large changes in neural encoding and/or in the recording itself.

Extending the shine-through effect to classical masking paradigms.

A vernier, presented for a short time, shines through a following grating if the grating contains nine and more elements but remains largely invisible for smaller gratings. Therefore, extended grating masks yield, surprisingly, less masking than smaller ones. Here, we show that this mask size effect is not unique to grating masks. Masking diminishes if the size of classical pattern-, noise-, light-, and metacontrast masks increases and if these masks are regular, i.e. highly ordered.

Local interactions in neural networks explain global effects in Gestalt processing and masking.

One of the fundamental and puzzling questions in vision research is how objects are segmented from their backgrounds and how object formation evolves in time. The recently discovered shine-through effect allows one to study object segmentation and object formation of a masked target depending on the spatiotemporal Gestalt of the masking stimulus (Herzog & Koch, 2001). In the shine-through effect, a vernier (two abutting lines) precedes a grating for a very short time. For small gratings, the vernier remains invisible while it regains visibility as a shine-through element for extended and homogeneous gratings. However, even subtle deviations from the homogeneity of the grating diminish or even abolish shine-through. At first glance, these results suggest that explanations of these effects have to rely on high-level Gestalt terminology such as homogeneity rather than on low-level properties such as luminance (Herzog, Fahle, & Koch, 2001). Here, we show that a simple neural network model of the Wilson-Cowan type qualitatively and quantitatively explains the basic effects in the shine-through paradigm, although the model does not contain any explicit, global Gestalt processing. Visibility of the target vernier corresponds to transient activation of neural populations resulting from the dynamics of local lateral interactions of excitatory and inhibitory layers of neural populations.

Finite-size effects of avalanche dynamics.

We study the avalanche dynamics of a system of globally coupled threshold elements receiving random input. The model belongs to the same universality class as the random-neighbor version of the Olami-Feder-Christensen stick-slip model. A closed expression for avalanche size distributions is derived for arbitrary system sizes N using geometrical arguments in the system's configuration space. For finite systems, approximate power-law behavior is obtained in the nonconservative regime, whereas for N--> infinity, critical behavior with an exponent of -3/2 is found in the conservative case only. We compare these results to the avalanche properties found in networks of integrate-and-fire neurons, and relate the different dynamical regimes to the emergence of synchronization with and without oscillatory components.