Detlef Wegener

The Influence of Sustained Selective Attention on Stimulus Selectivity in Macaque Visual Area MT

Remarkable alterations of perception during long-lasting attentional processes have been described in several recent studies. Although these findings have gained much interest, almost nothing is known about the modulation of neuronal responses during sustained attention. Therefore, we investigated the effect of prolonged selective attention on neuronal feature selectivity. Awake macaque monkeys were trained to perform a motion-tracking task that required attending one of two simultaneously presented moving bars for up to 15 sec. Extracellular recordings were obtained from neurons in macaque motion-sensitive middle temporal visual area (MT/V5). Under conditions of attention, we found high and constant direction selectivity over time. This was expressed by a strong and persistent response contrast between presentations of preferred and nonpreferred stimuli in successive motion cycles. With attention directed to another moving bar, neuronal responses to the behaviorally irrelevant stimulus became continuously less specific for the direction of motion. In particular, increasingly higher firing rates for motion in null direction caused a strong reduction of direction selectivity, which further increased with enhanced proximity between target and distracter bar. A passive condition experiment revealed that this reduction occurred only when motion remained the behaviorally relevant feature but disappeared when attention was withdrawn from this feature domain. Thus, sustained attention seems to stabilize direction selectivity of neurons in area MT against a time and competition-dependent degradation, whereas nonattended objects suffer from a reduced neuronal representation.

Feature-based attention and the suppression of non-relevant object features

Feature-directed attention has been recently studied in various psychophysical, electrophysiological, and imaging studies. Convincing evidence has been obtained for its global effectiveness, but there is a debate about the processing fate of non-attended target features. A number of studies demonstrated feature-directed attention being associated with co-selection of non-relevant object features, thus resulting in selection of the entire object, whereas most other studies did not examine the extent to which processing of non-attended features was affected. Here, we present the results of two psychophysical experiments consisting of a Posner-like paradigm in which subjects were cued either to an individual feature or the entire object. We measured reaction times to changes in speed or colour of one of two simultaneously presented gratings. Our results strongly support the view that feature-based selection is a unique selection process different from object-based selection in that it can be associated with active suppression of non-relevant features.

Monkey area MT latencies to speed changes depend on attention and correlate with behavioral reaction times.

Selective visual attention is known to be associated with characteristic modulations of neuronal activity in early visual cortex, but there is only rare evidence showing that these neuronal modulations are directly related to attention-dependent behavioral improvements. Here, we describe a strong, transient increase in the response of neurons in the mediotemporal (MT) area to behaviorally relevant speed changes that is not only modulated by attention but also highly correlated with the animals performance. In trials with fast reaction time (RT), this transient component occurs with short latency, whereas latency increases monotonically with slower RT. Importantly, RTs are related not to the firing rate modulation during sustained attentive tracking of the target prior to the speed change but to the variability of the neuronal response. Our findings suggest a direct link between attention-dependent response modulations in early visual cortex and improved behavioral performance.

Speed change detection in foveal and peripheral vision.

Perception of constant motion has been extensively studied both psychophysically and physiologically, but the human ability to detect dynamic changes in motion, such as rapid speed changes, is only poorly characterized and understood. Yet, perception and representation of such dynamic changes is of strong behavioral relevance, as illustrated by their potential for attentional capture. In the present study, we measured and compared detection thresholds for instantaneous accelerations and decelerations of drifting Gabor patches at different retinal eccentricities. As a main result, we find that detection performance depends strongly on eccentricity. Under foveal viewing conditions, average thresholds were lower for accelerations than for decelerations. However, between 5° and 15° eccentricity, this relation is inverted, and deceleration detection becomes better than acceleration detection. Results of an additional experiment suggest that this can be explained by a fast eccentricity-dependent adaptation effect. Our findings are discussed with special emphasis on their relation to data from neurophysiological experiments.

A new type of recording chamber with an easy-to-exchange microdrive array for chronic recordings in macaque monkeys

In monkeys, long-term recordings with chronically implanted microelectrodes frequently suffer from a continuously decreasing probability to record single units or even small multiunit clusters. This problem is associated with two technical limitations of the available devices: first, restrictions for electrode movement, and second, absent possibility to exchange electrodes easily on a regular basis. Permitting to adjust the recording site and to use new recording tracks with proper electrodes may avoid these problems and make chronic more similar to acute recordings. Here, we describe a novel type of implant tackling this issue. It consists of a new type of recording chamber combined with an exchangeable multielectrode array that precisely fits into it. The multielectrode array is reversibly fixed to the chamber, and within a minute it can be exchanged against another array equipped with new electrodes at the awake animal. The array allows for bidirectional movement of six electrodes for a distance of up to 12 mm. The recording chamber enables hermetical isolation of the intracranial space, resulting in long-lasting aseptic conditions and reducing dural thickening to a minimum, as confirmed by microbiological and histopathological analysis. The device has a simple design and is both easy to produce and low in cost. Functionality has been tested in primary and secondary visual cortex of three macaque monkeys over a period of up to 15 mo. The results show that even after more than a year, single and multiunit responses can be obtained with high incidence.

Selective visual attention ensures constancy of sensory representations: Testing the influence of perceptual load and spatial competition

We report findings from several variants of a psychophysical experiment using an acceleration detection task in which we tested predictions derived from recent neurophysiological data obtained from monkey area MT. The task was designed as a Posner paradigm and required subjects to detect the speed-up of a moving bar, cued with 75% validity. Displays varied according to number of simultaneously presented objects, spatial distance, and difficulty of the task. All data obtained under different levels of competition with multiple objects were compared to a corresponding condition, in which only a single moving bar was presented in the absence of any interfering distracter object. For attended objects, subjects did not show any difference in their ability to detect accelerations, regardless of the strength of inter-object competition or spatial distance. This finding was consistent in all of the experiments, and was even obtained when the acceleration was made hardly detectable. In contrast, increasing competitive interactions either by enhancing number of objects or spatial proximity resulted in strong reduction of performance for non-attended objects. The findings support current noise reduction models and suggest that attention adjusts neuronal processing to ensure a constant sensory representation of the attended object as if this object was the only one in the scene.

Attentional spreading to task-irrelevant object features: experimental support and a 3-step model of attention for object-based selection and feature-based processing modulation

Directing attention to a specific feature of an object has been linked to different forms of attentional modulation. Object-based attention theory founds on the finding that even task-irrelevant features at the selected object are subject to attentional modulation, while feature-based attention theory proposes a global processing benefit for the selected feature even at other objects. Most studies investigated either the one or the other form of attention, leaving open the possibility that both object- and feature-specific attentional effects do occur at the same time and may just represent two sides of a single attention system. We here investigate this issue by testing attentional spreading within and across objects, using reaction time (RT) measurements to changes of attended and unattended features on both attended and unattended objects. We asked subjects to report color and speed changes occurring on one of two overlapping random dot patterns (RDPs), presented at the center of gaze. The key property of the stimulation was that only one of the features (e.g., motion direction) was unique for each object, whereas the other feature (e.g., color) was shared by both. The results of two experiments show that co-selection of unattended features even occurs when those features have no means for selecting the object. At the same time, they demonstrate that this processing benefit is not restricted to the selected object but spreads to the task-irrelevant one. We conceptualize these findings by a 3-step model of attention that assumes a task-dependent top-down gain, object-specific feature selection based on task- and binding characteristics, and a global feature-specific processing enhancement. The model allows for the unification of a vast amount of experimental results into a single model, and makes various experimentally testable predictions for the interaction of object- and feature-specific processes.

Task-specific, dimension-based attentional shaping of motion processing in monkey area MT

Nonspatially selective attention is based on the notion that specific features or objects in the visual environment are effectively prioritized in cortical visual processing. Feature-based attention (FBA), in particular, is a well-studied process that dynamically and selectively addresses neurons preferentially processing the attended feature attribute (e.g., leftward motion). In everyday life, however, behavior may require high sensitivity for an entire feature dimension (e.g., motion), but experimental evidence for a feature dimension-specific attentional modulation on a cellular level is lacking. Therefore, we investigated neuronal activity in macaque motion-selective mediotemporal area (MT) in an experimental setting requiring the monkeys to detect either a motion change or a color change. We hypothesized that neural activity in MT is enhanced when the task requires perceptual sensitivity to motion. In line with this, we found that mean firing rates were higher in the motion task and that response variability and latency were lower compared with values in the color task, despite identical visual stimulation. This task-specific, dimension-based modulation of motion processing emerged already in the absence of visual input, was independent of the relation between the attended and stimulating motion direction, and was accompanied by a spatially global reduction of neuronal variability. The results provide single-cell support for the hypothesis of a feature dimension-specific top-down signal emphasizing the processing of an entire feature class.NEW & NOTEWORTHY Cortical processing serving visual perception prioritizes information according to current task requirements. We provide evidence in favor of a dimension-based attentional mechanism addressing all neurons that process visual information in the task-relevant feature domain. Behavioral tasks required monkeys to attend either color or motion, causing modulations of response strength, variability, latency, and baseline activity of motion-selective monkey area MT neurons irrespective of the attended motion direction but specific to the attended feature dimension.

Human feature-based attention consists of two distinct spatiotemporal processes

In human and nonhuman primates, goal-directed behavior requires the selection of relevant pieces of information from the multitude of simultaneous sensory inputs. Feature-based attention (FBA) plays a crucial role in this selection by improving the neuronal representation of an attended stimulus feature. Of particular interest for understanding the neuronal mechanisms behind FBA is the processing fate of spatially unattended stimuli, either sharing the attended feature attribute or belonging to the attended or to a nonattended feature dimension. Using a wide range of cue/stimulus combinations, we investigated event-related potentials from the human brain, recorded under conditions of different feature attention but constant visual stimulation. We found that neural processing of visual stimuli sharing the dimension or the attribute of the attended target is associated with two distinct spatiotemporal processes, particularly prominent during the selection negativity period. Dimension-based modulation of neural signals first emerged over frontal electrode sites, and temporally preceded and accompanied attribute-specific FBA effects at occipital, parieto-occipital, and parietal electrodes. The findings suggest a process of FBA that not only increases responses of those neurons particularly tuned to the attended attribute but also modulates activity in the cortical module that is selective for the feature dimension to which the attended attribute belongs.

Transient activity in monkey area MT represents speed changes and is correlated with human behavioral performance

Neurons in the middle temporal area (MT) respond to motion onsets and speed changes with a transient-sustained firing pattern. The latency of the transient response has recently been shown to correlate with reaction time in a speed change detection task, but it is not known how the sign, the amplitude, and the latency of this response depend on the sign and the magnitude of a speed change, and whether these transients can be decoded to explain speed change detection behavior. To investigate this issue, we measured the neuronal representation of a wide range of positive and negative speed changes in area MT of fixating macaques and obtained three major findings. First, speed change transients not only reflect a neurons absolute speed tuning but are shaped by an additional gain that scales the tuned response according to the magnitude of a relative speed change. Second, by means of a threshold model positive and negative population transients of a moderate number of MT neurons explain detection of both positive and negative speed changes, respectively, at a level comparable to human detection rates under identical visual stimulation. Third, like reaction times in a psychophysical model of velocity detection, speed change response latencies follow a power-law function of the absolute difference of a speed change. Both this neuronal representation and its close correlation with behavioral measures of speed change detection suggest that neuronal transients in area MT facilitate the detection of rapid changes in visual input.