Neural responses to natural visual motion are spatially selective across the visual field, with selectivity differing across brain areas and task.

It is well established that neural responses to visual stimuli are enhanced at select locations in the visual field. Although spatial selectivity and the effects of spatial attention are well understood for discrete tasks (e.g. visual cueing), little is known for naturalistic experience that involves continuous dynamic visual stimuli (e.g. driving). Here, we assess the strength of neural responses across the visual space during a kart-race game. Given the varying relevance of visual location in this task, we hypothesized that the strength of neural responses to movement will vary across the visual field, and it would differ between active play and passive viewing. To test this, we measure the correlation strength of scalp-evoked potentials with optical flow magnitude at individual locations on the screen. We find that neural responses are strongly correlated at task-relevant locations in visual space, extending beyond the focus of overt attention. Although the driver's gaze is directed upon the heading direction at the centre of the screen, neural responses were robust at the peripheral areas (e.g. roads and surrounding buildings). Importantly, neural responses to visual movement are broadly distributed across the scalp, with visual spatial selectivity differing across electrode locations. Moreover, during active gameplay, neural responses are enhanced at select locations in the visual space. Conventionally, spatial selectivity of neural response has been interpreted as an attentional gain mechanism. In the present study, the data suggest that different brain areas focus attention on different portions of the visual field that are task-relevant, beyond the focus of overt attention.

During natural viewing, neural processing of visual targets continues throughout saccades.

Relatively little is known about visual processing during free-viewing visual search in realistic dynamic environments. Free-viewing is characterized by frequent saccades. During saccades, visual processing is thought to be suppressed, yet we know that the presaccadic visual content can modulate postsaccadic processing. To better understand these processes in a realistic setting, we study here saccades and neural responses elicited by the appearance of visual targets in a realistic virtual environment. While subjects were being driven through a 3D virtual town, they were asked to discriminate between targets that appear on the road. Using a system identification approach, we separated overlapping and correlated activity evoked by visual targets, saccades, and button presses. We found that the presence of a target enhances early occipital as well as late frontocentral saccade-related responses. The earlier potential, shortly after 125 ms post-saccade onset, was enhanced for targets that appeared in the peripheral vision as compared to the central vision, suggesting that fast peripheral processing initiated before saccade onset. The later potential, at 195 ms post-saccade onset, was strongly modulated by the visibility of the target. Together these results suggest that, during natural viewing, neural processing of the presaccadic visual stimulus continues throughout the saccade, apparently unencumbered by saccadic suppression.

Visually evoked responses are enhanced when engaging in a video game.

While it is well known that vision guides movement, less appreciated is that the motor cortex also provides input to the visual system. Here, we asked whether neural processing of visual stimuli is acutely modulated during motor activity, hypothesizing that visual evoked responses are enhanced when engaged in a motor task that depends on the visual stimulus. To test this, we told participants that their brain activity was controlling a video game that was in fact the playback of a prerecorded game. The deception, which was effective in half of participants, aimed to engage the motor system while avoiding evoked responses related to actual movement or somatosensation. In other trials, subjects actively played the game with keyboard control or passively watched a playback. The strength of visually evoked responses was measured as the temporal correlation between the continuous stimulus and the evoked potentials on the scalp. We found reduced correlation during passive viewing, but no difference between active and sham play. Alpha-band (8-12 Hz) activity was reduced over central electrodes during sham play, indicating recruitment of motor cortex despite the absence of overt movement. To account for the potential increase of attention during gameplay, we conducted a second study with subjects counting screen items during viewing. We again found increased correlation during sham play, but no difference between counting and passive viewing. While we cannot fully rule out the involvement of attention, our findings do demonstrate an enhancement of visual evoked responses during active vision.

Extracting multidimensional stimulus-response correlations using hybrid encoding-decoding of neural activity.

In neuroscience, stimulus-response relationships have traditionally been analyzed using either encoding or decoding models. Here we propose a hybrid approach that decomposes neural activity into multiple components, each representing a portion of the stimulus. The technique is implemented via canonical correlation analysis (CCA) by temporally filtering the stimulus (encoding) and spatially filtering the neural responses (decoding) such that the resulting components are maximally correlated. In contrast to existing methods, this approach recovers multiple correlated stimulus-response pairs, and thus affords a richer, multidimensional analysis of neural representations. We first validated the technique's ability to recover multiple stimulus-driven components using electroencephalographic (EEG) data simulated with a finite element model of the head. We then applied the technique to real EEG responses to auditory and audiovisual narratives experienced identically across subjects, as well as uniquely experienced video game play. During narratives, both auditory and visual stimulus-response correlations (SRC) were modulated by attention and tracked inter-subject correlations. During video game play, SRC varied with game difficulty and the presence of a dual task. Interestingly, the strongest component extracted for visual and auditory features of film clips had nearly identical spatial distributions, suggesting that the predominant encephalographic response to naturalistic stimuli is supramodal. The diversity of these findings demonstrates the utility of measuring multidimensional SRC via hybrid encoding-decoding.

Attention Strongly Modulates Reliability of Neural Responses to Naturalistic Narrative Stimuli.

Attentional engagement is a major determinant of how effectively we gather information through our senses. Alongside the sheer growth in the amount and variety of information content that we are presented with through modern media, there is increased variability in the degree to which we "absorb" that information. Traditional research on attention has illuminated the basic principles of sensory selection to isolated features or locations, but it provides little insight into the neural underpinnings of our attentional engagement with modern naturalistic content. Here, we show in human subjects that the reliability of an individual's neural responses with respect to a larger group provides a highly robust index of the level of attentional engagement with a naturalistic narrative stimulus. Specifically, fast electroencephalographic evoked responses were more strongly correlated across subjects when naturally attending to auditory or audiovisual narratives than when attention was directed inward to a mental arithmetic task during stimulus presentation. This effect was strongest for audiovisual stimuli with a cohesive narrative and greatly reduced for speech stimuli lacking meaning. For compelling audiovisual narratives, the effect is remarkably strong, allowing perfect discrimination between attentional state across individuals. Control experiments rule out possible confounds related to altered eye movement trajectories or order of presentation. We conclude that reliability of evoked activity reproduced across subjects viewing the same movie is highly sensitive to the attentional state of the viewer and listener, which is aided by a cohesive narrative.