Human Experimental Studies on Attention

Several studies have been published that have contributed to the Selective Tuning model and a number are in progress. Each of the published ones is summarized below.

The work below was only possible because of a terrific string of post-doctoral fellows in my lab (Florin Cutzu, Daniel Loach, Michael Tombu), lab alumni Sean Culhane and Neil Bruce, research associate Eugene Simine, and a superb set of international collaborators (Nico Böhler, Ariel Schoenfeld, Hans-Joachim Heinze, Jens-Max Hopf, Alexandra Frischen, Juan Botella, Jesus Privado, and Steven Luck).

Böhler, C.N., Tsotsos, J.K., Schoenfeld, M., Heinze, H.-J., Hopf, J.-M., , The center-surround profile of the focus of attention arises from recurrent processing in visual cortex, Cerebral Cortex, (in press)

We recently demonstrated with magnetoencephalographic recordings in human observers that the focus of attention in visual search has a spatial profile consisting of a center enhancement surrounded by a narrow zone of sensory attenuation. Here, we report new data from 2 experiments providing insights into the cortical processes that cause the surround attenuation. We show that surround suppression appears in search tasks that require spatial scrutiny, that is the precise binding of search-relevant features at the target’s location but not in tasks that permit target discrimination without precise localization. Furthermore, we demonstrate that surround attenuation is linked with a stronger recurrent activity modulation in early visual cortex. Finally, we show that surround suppression appears with a delay (more than 175 ms) that is beyond the time course of the initial feedforward sweep of processing in the visual system. These observations together indicate that the suppressive surround is associated with recurrent processing and binding in the visual cortex.

Loach, D., Frischen, A., Bruce, N., Tsotsos, J.K., An attentional mechanism for selecting appropriate actions afforded by graspable objects, Psychological Science (in press).

An object may afford a number of different actions. Here we show that an attentional mechanism inhibits competing motor programs that could elicit erroneous actions. Participants made a speeded key press to categorise the second of two successively presented door-handles that were rotated at varying orientations relative to one another. Their responding hand was compatible or incompatible with the graspable part of the door-handles (right- or left-ward facing). Compatible responses were faster than incompatible responses if the two handles shared an identical orientation but were slower if the two handles were aligned at slightly dissimilar orientations. Such suppressive surround effects are hallmarks of attentional processing in the visual domain but have never been observed behaviourally in the motor domain. This finding delineates a common mechanism involved in two of the most important functions of the brain; to process sensory data and to prepare actions based on that information.

Loach, D., Botella, J., Privado, J., Tsotsos, J.K., Priming and Intrusion Errors in RSVP Streams with Two Response Dimensions, Psychological Research (published on line 30 May 2007) Volume 72, Number 3 / May, 2008, pages 281-288.

Loach and Marí-BeVa (Vis Cogn, 10:513–526, 2003) observed that a distractor stimulus, presented immediately after a behaviorally relevant target stimulus, negatively primed a related probe stimulus indicating that the distractor had been inhibited. They argued that “post-target inhibition” may be a mechanism for preventing interference from temporally proximal stimuli; interference that could potentially result in a binding/intrusion error. In order to test this hypothesis, the authors carried out two rapid serial visual presentation (RSVP) experiments in which participants had to report either the identity (Experiment 1) or color (Experiment 2) of a target letter surrounded by distractor letters. In Experiment 1, a close relationship between priming and errors was observed. When a distractor stimulus showed evidence of being inhibited the participant was less likely to commit a binding error. The opposite was true when a distractor stimulus showed evidence of being facilitated. The results of Experiment 2 showed limited evidence of the same relationship.

Tombu, M., Tsotsos, J.K., Attending to Orientation Results in an Inhibitory Surround in Orientation Space, Perception & Psychophysics, 2008, 70 (1), 30-35.

Subjects were required to attend to an orientation and make judgments about the stripes on briefly presented disks. Stripe orientation was varied so that they could be at, near, or far from the attended orientation. According to the selective-tuning model (Tsotsos, 1990; Tsotsos et al., 1995), attending to an orientation results in an

inhibitory surround for nearby orientations, but not for orientations farther away. In line with this prediction, the results revealed an inhibitory surround. As in the spatial domain, attending to a point in orientation space results in an inhibitory surround for nearby orientations.

Hopf, J.-M., Boehler C.N., Luck S.J., Tsotsos, J.K., Heinze, H.-J., Schoenfeld M.A., Direct neurophysiological evidence for spatial suppression surrounding the focus of attention in vision, Proceedings of the National Academy of Sciences, Biological Track 2006 Jan 24;103(4):1053-8. Epub 2006 Jan 12.

The spatial focus of attention has traditionally been envisioned as

a simple spatial gradient of enhanced activity that falls off monotonically

with increasing distance. Here, we show with high density magnetoencephalographic recordings in human observers that the focus of attention is not a simple monotonic gradient but instead contains an excitatory peak surrounded by a narrow inhibitory region. To demonstrate this center-surround profile, we asked subjects to focus attention onto a color pop-out target and then presented probe stimuli at various distances from the target.

We observed that the electromagnetic response to the probe was

enhanced when the probe was presented at the location of the target, but the probe response was suppressed in a narrow zone surrounding the target and then recovered at more distant locations. Withdrawing attention from the pop-out target by engaging observers in a demanding foveal task eliminated this pattern, confirming a truly attention-driven effect. These results indicate

that neural enhancement and suppression coexist in a spatially structured manner that is optimal to attenuate the most deleterious noise during visual object identification.

Cutzu, F., Tsotsos, J.K., The selective tuning model of visual attention: Testing the predictions arising from the inhibitory surround mechanism, Vision Research pp. 205 - 219, Jan. 2003.

The selective tuning model is a neurobiologically plausible neural network model of visual attention. One of its key predictions is that to simultaneously solve the problems of convergence of neural input and selection of attended items, the portions of the visual neural network that process an attended stimulus must be surrounded by inhibition. To test this hypothesis, we mapped the attentional field around an attended location in a matching task where the subject’s attention was directed to a cued target while the distance of a probe item to the target was varied systematically. The main result was that accuracy increased with inter-target separation. The observed pattern of variation of accuracy with distance provided strong evidence in favor of the critical prediction of the model that attention is actively inhibited in the immediate vicinity of an attended location.

Tsotsos, J.K., Culhane, S., Cutzu, F., From Theoretical Foundations to a Hierarchical Circuit for Selective Attention, Visual Attention and Cortical Circuits, p. 285 – 306, ed. by J. Braun, C. Koch, and J. Davis, MIT Press, 2001.

The goal was to map the variation of the attentional field around a target and discriminate between the predictions of the traditional models and of the selective tuning model. The principle of the experimental method was the following: direct the subjects' attention to a reference location in the visual field and concomitantly measure their ability to process visual information -- i.e., the intensity of the attentional field -- at different, probe locations of equal retinal resolution. By systematically varying the reference - probe distance, one can determine the dependence of the attentional field on distance to the focus of attention. The experimental requirements were threefold. (1) Engaging visual attention: the classical L - T discrimination task was used. Discrimination accuracy was employed as performance measure. (2) Directing the attention of the subject to one, pre-specified, reference target location: we resorted to pre-cueing. (3) Ensuring equal retinal resolution for all stimuli: we used a circular array display with fixation point in the center. A typical experimental sequence from left to right, consisted of cue image, test image, and mask. The cue, a light gray disk, anticipated the position of the reference target in the following test image. This will be referred to as the peripheral cue condition. It was shown for 180 msec, which is within the time range of effective cueing. The stimulus set in the test image consisted of six randomly oriented Ls and six randomly oriented Ts, arranged in random order on a ring. The characters were evenly spaced, and were overlaid on light gray disks as shown, middle panel. Two of the characters, the reference target and the probe target, were red (shown in the figures in bold) and the rest, the distractors, were black. The orientation of the imaginary line joining the two targets was randomly changed from trial to trial. The radius of the ring was 4° and character size was 0.6° visual angle. The task of the subject was to decide whether the two red characters were identical or different by pressing one of two keys on the computer keyboard. After 200 msec the test image was replaced by a mask consisting of red disks positioned at the locations of the disks enclosing the L and T characters in the preceding test image. The role of the mask was to erase the iconic memory of the target letters in the test display. It was during the mask that the subjects made their response. To ensure that all characters in the ring were perceived at same resolution, the subjects were instructed to always fixate the cross-hair in the center of the ring. The main variable of interest in this experiment was inter-target separation, taking on six distinct values, from one, when the two target characters were next neighbors, to six, when the targets were diametrically opposite. Each of the six inter-target separations was tested four times in the same condition and four times in the different condition. Thus, an experimental session included 24 same and 24 different trials.