Attention to Multiple Objects Facilitates Their Integration in Prefrontal and Parietal Cortex

• Published in: The Journal of neuroscience Vol. 37; no. 19; pp. 4942 - 4953
• Main Authors: Kim, Yee-Joon, Tsai, Jeffrey J, Ojemann, Jeffrey, Verghese, Preeti
• Format: Journal Article
• Language: English
• Published: United States Society for Neuroscience 10.05.2017
• Subjects: Adult; Attention - physiology; Cortex (parietal); Female; Humans; Integration; Male; Middle Aged; Nerve Net - physiology; Neural coding; Parietal Lobe - physiology; Pattern Recognition, Visual - physiology; Prefrontal cortex; Prefrontal Cortex - physiology; Space Perception - physiology; Task Performance and Analysis; Visual cortex; Visual evoked potentials; Visual stimuli; Young Adult; perceptual integration; electrocorticography; prefrontal cortex; attention to multiple objects; steady-state visual evoked potential
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.2370-16.2017

Selective attention is known to interact with perceptual organization. In visual scenes, individual objects that are distinct and discriminable may occur on their own, or in groups such as a stack of books. The main objective of this study is to probe the neural interaction that occurs between individual objects when attention is directed toward one or more objects. Here we record steady-state visual evoked potentials via electrocorticography to directly assess the responses to individual stimuli and to their interaction. When human participants attend to two adjacent stimuli, prefrontal and parietal cortex shows a selective enhancement of only the neural interaction between stimuli, but not the responses to individual stimuli. When only one stimulus is attended, the neural response to that stimulus is selectively enhanced in prefrontal and parietal cortex. In contrast, early visual areas generally manifest responses to individual stimuli and to their interaction regardless of attentional task, although a subset of the responses is modulated similarly to prefrontal and parietal cortex. Thus, the neural representation of the visual scene as one progresses up the cortical hierarchy becomes more highly task-specific and represents either individual stimuli or their interaction, depending on the behavioral goal. Attention to multiple objects facilitates an integration of objects akin to perceptual grouping. Individual objects in a visual scene are seen as distinct entities or as parts of a whole. Here we examine how attention to multiple objects affects their neural representation. Previous studies measured single-cell or fMRI responses and obtained only aggregate measures that combined the activity to individual stimuli as well as their potential interaction. Here, we directly measure electrocorticographic steady-state responses corresponding to individual objects and to their interaction using a frequency-tagging technique. Attention to two stimuli increases the interaction component that is a hallmark for perceptual integration of stimuli. Furthermore, this stimulus-specific interaction is represented in prefrontal and parietal cortex in a task-dependent manner.