Abstract

Focal visual attention typically produces enhanced perceptual processing at the psychological level and relatively stronger neural responses at the physiological level. A longstanding mechanistic question is whether these attentional effects pertain specifically to the attended (target) object or to the region of space it occupies. We show here that attentional response enhancement in macaque area V4 extends to behaviorally irrelevant objects in the vicinity of the target object, indicating that focal attention has a strong spatial component at the physiological level. In addition, we find that spatial attention effects typically show a striking directional asymmetry. The direction of the asymmetry varies between cells, so that some cells respond best when attention is directed to the left of the stimulus, some when attention is directed to the right, etc. Thus, attention involves not only enhanced responses to behavioral targets but also a complex modulation of responses to other stimuli in the surrounding visual space. : attention; visual; spatial; monkey; cortex; extrastriate; area V4 Extensive psychological research has shown that directed visual attention produces localized enhancement of perceptual processing. In some studies, this perceptual enhancement appears to be specific to the behavioral target object, so that other objects nearby or even overlapping in space are processed less effectively Key words We sought to dissociate the two factors and study spatial attention effects in isolation by means of a double-stimulus paradigm. One stimulus was a ring-shaped behavioral target used to control the locus of attention but was designed and positioned so as not to evoke a response from the cell under study. The other stimulus was a behaviorally irrelevant bar designed to evoke a strong response from the cell and was used to map the spatial profile of attention effects surrounding the ring target. Thus, the spatial position of the probe stimulus was dissociated from the position of the behavioral target. The locations of both stimuli were varied systematically so as to map the spatial profile of attentional modulation. Our results reveal a penumbra of attentional enhancement surrounding the behavioral target that affects responses to nearby behaviorally irrelevant stimuli. This supports the existence of a spatial mechanism of attention (without excluding the possibility of a coexisting object-based mechanism). In addition, for most V4 cells response strength depends on the direction in which attention lies relative to the receptive field, with the optimal direction varying between cells. This indicates that area V4 carries information about the positional relationship between stimulus and attention and suggests the emergence of an attention-centered reference frame for visual processing. A preliminary report of some of these results has been presented previously MATERIALS AND METHODS General. All surgical, training, and neurophysiological recording procedures conformed to National Institutes of Health and USDA guidelines and were carried out under an institutionally approved animal protocol using methods described previously Equipment. Visual stimuli were generated on an Iris Indigo workstation (SGI) and displayed on a 36 ϫ 27 cm color monitor with a resolution of 1280 ϫ 1024 pixels viewed at a distance of 55 cm. Single-unit activity in area V4 was recorded with 125-m-diameter epoxy-coated tungsten electrodes (A-M Systems) with impedances of 1-5 M⍀. Electrodes were inserted transdurally through a 5-mm-diameter craniotomy by means of a custom guide tube system. Electrode position was controlled by a stepping motor microdrive (Caltech Central Engineering Services). The electrical waveform was thresholded with a window discriminator, and the resulting digital signal was collected through the audio input channel of the Indigo workstation at a sample rate of 8 kHz. Eye position was monitored with a scleral search coil system (Remmel Labs) using the technique of Receptive field plotting. Macaque monkeys were seated before the display monitor in a standard primate chair with a response lever at-