Full Field Masking Causes Reversals in Perceived Event Order.

We generally experience a stable visual world in spite of regular disruptions caused by our own movements (saccades, blinks) or by the visual input itself (flashes, occlusions). In trying to understand the mechanisms responsible for this stability, saccades have been particularly well-studied, and a number of peri-saccadic perceptual distortions (spatial and temporal compression, failure to detect target displacement) have been explored. It has been shown that some of these distortions are not saccade specific, but also arise when the visual input is instead abruptly and briefly masked. Here, we demonstrate that another peri-saccadic distortion, the reversal of the temporal order of a pair of brief events, may also be found with masking. Human participants performed a temporal order judgment task, and the timing of stimuli and mask was varied over trials. Perceptual order was reversed on ~25% of the trials at the shortest stimulus to mask intervals. This was not merely a failure of target detection, since participants often reported these reversals with high subjective confidence. These findings update the constraints on models of stability around disruptions.

Theta-Gamma Coding Meets Communication-through-Coherence: Neuronal Oscillatory Multiplexing Theories Reconciled.

Several theories have been advanced to explain how cross-frequency coupling, the interaction of neuronal oscillations at different frequencies, could enable item multiplexing in neural systems. The communication-through-coherence theory proposes that phase-matching of gamma oscillations between areas enables selective processing of a single item at a time, and a later refinement of the theory includes a theta-frequency oscillation that provides a periodic reset of the system. Alternatively, the theta-gamma neural code theory proposes that a sequence of items is processed, one per gamma cycle, and that this sequence is repeated or updated across theta cycles. In short, both theories serve to segregate representations via the temporal domain, but differ on the number of objects concurrently represented. In this study, we set out to test whether each of these theories is actually physiologically plausible, by implementing them within a single model inspired by physiological data. Using a spiking network model of visual processing, we show that each of these theories is physiologically plausible and computationally useful. Both theories were implemented within a single network architecture, with two areas connected in a feedforward manner, and gamma oscillations generated by feedback inhibition within areas. Simply increasing the amplitude of global inhibition in the lower area, equivalent to an increase in the spatial scope of the gamma oscillation, yielded a switch from one mode to the other. Thus, these different processing modes may co-exist in the brain, enabling dynamic switching between exploratory and selective modes of attention.

The phase of ongoing EEG oscillations predicts the amplitude of peri-saccadic mislocalization.

Our constant eye movements mean that updating processes, such as saccadic remapping, are essential for the maintenance of a stable spatial representation of the world around us. It has been proposed that, rather than continually update a full spatiotopic map, only the location of a few key objects is updated, suggesting that the process is linked to attention. At the same time, mounting evidence links attention to oscillatory neuronal processes. We therefore hypothesized that updating processes should themselves show oscillatory characteristics, inherited from underlying attentional processes. To test this, we carried out a combined psychophysics and EEG experiment in human participants, using a saccadic mislocalization task as a behaviourally measureable proxy for spatial updating, and simultaneously recording 64-channel EEG. We then used a time-frequency analysis to test for a correlation between oscillation phase and perceptual outcome. We found a significant phase-dependence of mislocalization in a time-frequency region from around 400 ms prior to saccade initiation and peaking at around 7 Hz, principally apparent over occipital electrodes. Thus the degree of perceived mislocalization is correlated with the phase of a theta-frequency oscillation prior to saccade onset. We conclude that spatial updating processes are indeed linked to rhythmic processes in the brain.

Attention searches nonuniformly in space and in time.

Difficult search tasks are known to involve attentional resources, but the spatiotemporal behavior of attention remains unknown. Are multiple search targets processed in sequence or in parallel? We developed an innovative methodology to solve this notoriously difficult problem. Observers performed a difficult search task during which two probes were flashed at varying delays. Performance in reporting probes at each location was considered a measure of attentional deployment. By solving a second-degree equation, we determined the probability of probe report at the most and least attended probe locations on each trial. Because these values differed significantly, we conclude that attention was focused on one stimulus or subgroup of stimuli at a time, and not divided uniformly among all search stimuli. Furthermore, this deployment was modulated periodically over time at ∼ 7 Hz. These results provide evidence for a nonuniform spatiotemporal deployment of attention during difficult search.

Mechanisms for Rapid Adaptive Control of Motion Processing in Macaque Visual Cortex.

A key feature of neural networks is their ability to rapidly adjust their function, including signal gain and temporal dynamics, in response to changes in sensory inputs. These adjustments are thought to be important for optimizing the sensitivity of the system, yet their mechanisms remain poorly understood. We studied adaptive changes in temporal integration in direction-selective cells in macaque primary visual cortex, where specific hypotheses have been proposed to account for rapid adaptation. By independently stimulating direction-specific channels, we found that the control of temporal integration of motion at one direction was independent of motion signals driven at the orthogonal direction. We also found that individual neurons can simultaneously support two different profiles of temporal integration for motion in orthogonal directions. These findings rule out a broad range of adaptive mechanisms as being key to the control of temporal integration, including untuned normalization and nonlinearities of spike generation and somatic adaptation in the recorded direction-selective cells. Such mechanisms are too broadly tuned, or occur too far downstream, to explain the channel-specific and multiplexed temporal integration that we observe in single neurons. Instead, we are compelled to conclude that parallel processing pathways are involved, and we demonstrate one such circuit using a computer model. This solution allows processing in different direction/orientation channels to be separately optimized and is sensible given that, under typical motion conditions (e.g., translation or looming), speed on the retina is a function of the orientation of image components. SIGNIFICANCE STATEMENT: Many neurons in visual cortex are understood in terms of their spatial and temporal receptive fields. It is now known that the spatiotemporal integration underlying visual responses is not fixed but depends on the visual input. For example, neurons that respond selectively to motion direction integrate signals over a shorter time window when visual motion is fast and a longer window when motion is slow. We investigated the mechanisms underlying this useful adaptation by recording from neurons as they responded to stimuli moving in two different directions at different speeds. Computer simulations of our results enabled us to rule out several candidate theories in favor of a model that integrates across multiple parallel channels that operate at different time scales.

Long-range clustered connections within extrastriate visual area V5/MT of the rhesus macaque.

Visual area V5/MT in the rhesus macaque has a distinct functional organization, where neurons with specific preferences for direction of motion and binocular disparity are co-organized in columns or clusters. Here, we analyze the pattern of intrinsic connectivity within cortical area V5/MT in both parasagittal sections of the intact brain and tangential sections from flatmounted cortex using small injections of the retrograde tracer cholera toxin subunit b. Labeled cells were predominantly found in cortical layers 2, 3, and 6. Going along the cortical layers, labeled cells were concentrated in regularly spaced clusters. The clusters nearest to the injection site were approximately 2 mm from its center. In flatmounted cortex, along the dorsoventral axis of V5/MT, we identified further clusters of labeled cells up to 10 mm from the injection site. Quantitative analysis of parasagittal sections estimated average cluster spacing at 2.2 mm; in cortical flatmounts, spacing was 2.3 mm measured radially from the injection site. The results suggest a regular pattern of intrinsic connectivity within V5/MT, which is consistent with connectivity between sites with a common preference for both direction of motion and binocular depth. The long-range connections can potentially account for the large suppressive surrounds of V5/MT neurons.

Neuronal responses during and after the presentation of static visual stimuli in macaque primary visual cortex.

Viewing static visual scenes for several seconds or longer can induce a wide variety of striking percepts, including negative afterimages, fading, and motion aftereffects. To characterize the neuronal bases of such phenomena and elucidate functional circuitry in the visual system, we recorded responses of neurons in primary visual cortex (V1) of anesthetized macaques during and after the presentation of prolonged static visual stimuli. We found that 72% of cells generated significant after-responses (ARs) that outlasted classical off-transients after the cessation of stimuli, and AR amplitude grew with stimulus duration. After the longest stimuli tested (32 s), the amplitude and the time course of the AR were on average comparable to, and correlated with, those of the maintained response evoked while stimuli were present. These observations generally held regardless of cell class: simple, complex, direction selective (DS) or non-DS. The average decay time constant of the AR for orientation-tuned cells was 0.65 s. This is strikingly shorter than time constants observed in the lateral geniculate nucleus, which were on the order of tens of seconds. Cells in V1 that lacked orientation tuning displayed an intermediate time course, with a mean time constant of 4.3 s. These results are consistent with a multistage model in which cells at successive stages adapt to their inputs with progressively shorter time constants. Our findings suggest that the perceptual phenomena of fading and afterimages are shaped by both cortical and subcortical dynamics and provide a physiological framework for the interpretation of recent and long-standing psychophysical observations.

Responses to static visual images in macaque lateral geniculate nucleus: implications for adaptation, negative afterimages, and visual fading.

Adaptation to static scenes is a familiar and fundamental aspect of visual perception that causes negative afterimages, fading, and many other visual illusions. To establish a foundation for understanding the neuronal bases of such phenomena and to constrain the contributions of retinal versus cortical processing, we studied the responses of neurons in the dorsal lateral geniculate nucleus during and after the presentation of prolonged static visual stimuli. We found that parvocellular (P) cells (the more numerous and color-sensitive pathway) showed response adaptation with a time constant on the order of tens of seconds and that their response after the removal of a visual stimulus lasting 1 min was similar in amplitude and time course to the response evoked by the photographic negative stimulus. Magnocellular (M) cells (the faster-conducting and achromatic pathway) had after responses that were substantially weaker than responses evoked by patterned visual stimuli. This difference points to the existence of an adaptive mechanism in the P-pathway that is absent or impaired in the M-pathway and is inconsistent with full adaptation of photoreceptors, which feed both pathways. Cells in both pathways often maintained a substantial tonic response throughout 1 min stimuli, suggesting that these major feedforward inputs to cortex adapt too slowly to account for visual fading. Our findings suggest that faster-adapting mechanisms in cortex are likely to be required to account for the dynamics of perception during and after the viewing of prolonged static images.

Neuronal oscillations and the rate-to-phase transform: mechanism, model and mutual information.

Theoretical and experimental studies suggest that oscillatory modes of processing play an important role in neuronal computations. One well supported idea is that the net excitatory input during oscillations will be reported in the phase of firing, a 'rate-to-phase transform', and that this transform might enable a temporal code. Here, we investigate the efficiency of this code at the level of fundamental single cell computations. We first develop a general framework for the understanding of the rate-to-phase transform as implemented by single neurons. Using whole cell patch-clamp recordings of rat hippocampal pyramidal neurons in vitro, we investigated the relationship between tonic excitation and phase of firing during simulated theta frequency (5 Hz) and gamma frequency (40 Hz) oscillations, over a range of physiological firing rates. During theta frequency oscillations, the phase of the first spike per cycle was a near-linear function of tonic excitation, advancing through a full 180 deg, from the peak to the trough of the oscillation cycle as excitation increased. In contrast, this relationship was not apparent for gamma oscillations, during which the phase of firing was virtually independent of the level of tonic excitatory input within the range of physiological firing rates. We show that a simple analytical model can substantially capture this behaviour, enabling generalization to other oscillatory states and cell types. The capacity of such a transform to encode information is limited by the temporal precision of neuronal activity. Using the data from our whole cell recordings, we calculated the information about the input available in the rate or phase of firing, and found the phase code to be significantly more efficient. Thus, temporal modes of processing can enable neuronal coding to be inherently more efficient, thereby allowing a reduction in processing time or in the number of neurons required.

Cortical songs revisited: a lesson in statistics.

Recordings from single neurons in the cortex have revealed precisely repeating patterns of synaptic events. These repeats are known as cortical "motifs" and have been suggested to reflect the precise replay of spatiotemporal firing sequences ("synfire" chains). In this issue of Neuron, Mokeichev et al. use compelling statistical analysis to show that, rather than being evidence of deterministic synfire chains, such cortical motifs are bound to appear by chance due to the natural dynamics of voltage fluctuations in neurons.