Bart Krekelberg

Adaptation: from single cells to BOLD signals

Functional magnetic resonance imaging adaptation (fMRIa) is an increasingly popular method that aims to provide insight into the functional properties of subpopulations of neurons within an imaging voxel. The technique relies on the assumption that neural adaptation reduces activity when two successive stimuli activate the same subpopulation but not when they stimulate different subpopulations. Here, we assess the validity of fMRIa by comparing single-cell recordings with functional imaging of orientation, motion and face processing. We find that fMRIa provides novel insight into neural representations in the human brain. However, network responses in general and adaptation in particular are more complex than is often assumed, and an unequivocal interpretation of fMRIa results can be achieved only with great care.

Postsaccadic visual references generate presaccadic compression of space

With every rapid gaze shift (saccade), our eyes experience a different view of the world. Stable perception of visual space requires that points in the new image are associated with corresponding points in the previous image. The brain may use an extraretinal eye position signal to compensate for gaze changes, or, alternatively, exploit the image contents to determine associated locations. Support for a uniform extraretinal signal comes from findings that the apparent position of objects briefly flashed around the time of a saccade is often shifted in the direction of the saccade. This view is challenged, however, by observations that the magnitude and direction of the displacement varies across the visual field. Led by the observation that non-uniform displacements typically occurred in studies conducted in slightly illuminated rooms, here we determine the dependence of perisaccadic mislocalization on the availability of visual spatial references at various times around a saccade. We find that presaccadic compression occurs only if visual references are available immediately after, rather than before or during, the saccade. Our findings indicate that the visual processes of transsaccadic spatial localization use mainly postsaccadic visual information.

Neural correlates of implied motion

Current views of the visual system assume that the primate brain analyses form and motion along largely independent pathways; they provide no insight into why form is sometimes interpreted as motion. In a series of psychophysical and electrophysiological experiments in humans and macaques, here we show that some form information is processed in the prototypical motion areas of the superior temporal sulcus (STS). First, we show that STS cells respond to dynamic Glass patterns, which contain no coherent motion but suggest a path of motion. Second, we show that when motion signals conflict with form signals suggesting a different path of motion, both humans and monkeys perceive motion in a compromised direction. This compromise also has a correlate in the responses of STS cells, which alter their direction preferences in the presence of conflicting implied motion information. We conclude that cells in the prototypical motion areas in the dorsal visual cortex process form that implies motion. Estimating motion by combining motion cues with form cues may be a strategy to deal with the complexities of motion perception in our natural environment.

Neural dynamics of saccadic suppression.

We make fast, ballistic eye movements called saccades more often than our heart beats. Although every saccade causes a large movement of the image of the environment on our retina, we never perceive this motion. This aspect of perceptual stability is often referred to as saccadic suppression: a reduction of visual sensitivity around the time of saccades. Here, we investigated the neural basis of this perceptual phenomenon with extracellular recordings from awake, behaving monkeys in the middle temporal, medial superior temporal, ventral intraparietal, and lateral intraparietal areas. We found that, in each of these areas, the neural response to a visual stimulus changes around an eye movement. The perisaccadic response changes are qualitatively different in each of these areas, suggesting that they do not arise from a change in a common input area. Importantly, our data show that the suppression in the dorsal stream starts well before the eye movement. This clearly shows that the suppression is not just a consequence of the changes in visual input during the eye movement but rather must involve a process that actively modulates neural activity just before a saccade.

Temporal recruitment along the trajectory of moving objects and the perception of position

The trajectory of a moving object provides information about its velocity, direction and position. This information can be used to enhance the visual systems ability to detect changes in these parameters. We show that the visibility of the trajectory of a moving object influences the perception of its position. This form of temporal recruitment builds up on a long timescale of approximately 500 ms. Temporary occlusion of the trajectory during this time period reduces recruitment, but does not abolish it. Moreover, we found no spatial restrictions on recruitment on the scale of 10 degrees of arc. When the position of objects on trajectories with different degrees of visibility are compared, this recruitment effect causes spatial offsets. This leads to a visual illusion in which the position of moving objects is misperceived.

Visual perception and saccadic eye movements

We use saccades several times per second to move the fovea between points of interest and build an understanding of our visual environment. Recent behavioral experiments show evidence for the integration of pre- and postsaccadic information (even subliminally), the modulation of visual sensitivity, and the rapid reallocation of attention. The recent physiological literature has identified a characteristic modulation of neural responsiveness-perisaccadic reduction followed by a postsaccadic increase-that is found in many visual areas, but whose source is as yet unknown. This modulation seems optimal for reducing sensitivity during and boosting sensitivity between saccades, but no study has yet established a direct causal link between neural and behavioral changes.

Interactions between Speed and Contrast Tuning in the Middle Temporal Area: Implications for the Neural Code for Speed

A car driving through the fog appears to move more slowly than one driving on a clear and sunny day. In the laboratory, this observation has been confirmed as a pronounced reduction of perceived speed caused by a reduction in contrast. We measured the influence of contrast on cells in the middle temporal area (MT) of the macaque, which has been hypothesized to underlie the perception of speed. The influence of contrast on the responsiveness and speed tuning of these cells was pervasive and highly regular. As expected, most cells responded less at low contrast. More importantly, the preferred speed of most cells shifted to lower speeds at lower contrasts. Moreover, approximately one-third of cells surprisingly responded more strongly to slow low-contrast stimuli than to slow high-contrast stimuli. Current models of speed perception suggest that each MT cell votes for its preferred speed, with a vote determined by its firing rate. We tested a number of these labeled-line models by entering the neural responses we recorded from MT and comparing the predictions of the models with the perceptual reports of human subjects and monkeys. Contrary to the perceptual reports, the labeled-line models predicted that perceived speed should increase when contrast is decreased. We therefore conclude that perceived speed is not based on a labeled-line interpretation of MT cells.

Neural correlates of saccadic suppression in humans.

When you look into a mirror and move your eyes left to right, you will see that you cannot observe your own eye movements. This demonstrates the phenomenon of saccadic suppression: during saccadic eye movements, visual sensitivity is much reduced. Given that humans make more than 100,000 eye movements each day, it is clear why suppression is needed: without it, the motion on the retina would prevent us from seeing anything at all. Psychophysical data show that suppression is stimulus selective: it is strongest for the kind of stimuli that preferentially activate magnocellular thalamic neurons. This has led to the hypothesis that saccadic suppression selectively targets the magnocellular stream. We used fMRI to find brain areas with a stimulus-selective suppression of the BOLD signal that matches the psychophysical data. We found such a neural correlate of saccadic suppression in the dorsal stream (hMT+, V7) and in ventral area V4. These areas receive magnocellular input; hence our findings are consistent with the magnocellular hypothesis. The range of effects in our data and in single cell data, however, argues against a single thalamic mechanism that suppresses all cortical input. Instead, we speculate that saccadic suppression relies on multiple mechanisms operating in different cortical areas.

Linking form and motion in the primate brain

Understanding dynamic events entails the integration of information about form and motion that is crucial for fast and successful interactions in complex environments. A striking example of our sensitivity to dynamic information is our ability to recognize animate figures by the way they move and infer motion from still images. Accumulating evidence for form and motion interactions contrasts with the traditional dissociation between shape and motion-related processes in the ventral and dorsal visual pathways. By combining findings from physiology and brain imaging it can be demonstrated that the primate brain converts information about spatiotemporal sequences into meaningful actions through interactions between early and higher visual areas processing form and motion and frontal-parietal circuits involved in the understanding of actions.

Neural Correlates of Visual Localization and Perisaccadic Mislocalization

While reading this text, your eyes jump from word to word. Yet you are unaware of the motion this causes on your retina; the brain somehow compensates for these displacements and creates a stable percept of the world. This compensation is not perfect; perisaccadically, perceptual space is distorted. We show that this distortion can be traced to a representation of retinal position in the medial temporal and medial superior temporal areas. These cells accurately represent retinal position during fixation, but perisaccadically, the same cells distort the representation of space. The time course and magnitude of this distortion are similar to the mislocalization found psychophysically in humans. This challenges the assumption in many psychophysical studies that the perisaccadic retinal position signal is veridical.