Load Dependence of β and γ Oscillations Predicts Individual Capacity of Visual Attention

Abstract

Human capability to concurrently attend and perceive multiple visual objects has a limited and individual capacity of 2-4 objects. Neuronal mechanisms that support the perception of multiple objects and underlie these attentional capacity limits have remained unclear. We investigated the role of neuronal oscillations in multiobject visual perception and in limiting the attentional capacity. To this end, we used parametric multiobject tracking tasks, MEG and EEG recordings, and data-driven source-space analyses to localize the neuronal substrates of task performance. Three lines of evidence suggested a mechanistic role for neuronal oscillations in multiobject attention. First, oscillation amplitudes preceding target events were distinct for subsequently detected and undetected targets and also predicted reaction times to the target events. Second, suppression of to low-␤ (Ͻ20 Hz) and strengthening of high-␤ to ␥ (20 -90 Hz) oscillations in frontoparietal and visual regions were correlated with attentional load. Third, the load-dependent strengthening of ␥ (30 -90 Hz) band oscillations in lateral prefrontal, posterior parietal, and visual cortices predicted interindividual variability in attentional capacity. A progressive recruitment of ␥ oscillations in sensory, attentional, and executive networks is thus directly correlated with multiobject attentional demands and, in particular, with the individual capability to consciously attend and perceive multiple visual objects concurrently. These data support the hypothesis that ␥ oscillations contribute both to neuronal object representations and to attentional and executive processing.

Targeting Oxidative Stress and Aberrant Critical Period Plasticity in the Developmental Trajectory to Schizophrenia

“…Therefore, dysfunction of the PVI network may lead to abnormal neuronal activity in patients, including oscillatory activity within θ, β, and γ ranges. [36][37][38] Ultimately, interneuron dysfunction could contribute to altered sensory perception, 39 deficits in working memory, 18,40 attention, 41 and learning. 42 Recent studies have revealed anomalies in hippocampal and/or prefrontal PVI in many preclinical animal models aiming to reproduce genetic vulnerabilities [43][44][45][46] or environmental risk factors 47 such as prenatal maternal stress, 48 maternal and perinatal immune challenge, 49,50 hypoxia, 51,52 early-life iron deficiency, 53 maternal separation, 54 and social isolation.…”

The Role of Local and Large-Scale Neuronal Synchronization in Human Cognition

“…Modified from ref (Hirvonen and Palva 2016) capacity limitations of visual attention ( Fig. 2a) (Rouhinen et al 2013). The localization of the load dependency of gamma oscillations revealed a network of active areas in the visual cortex but even more so also in frontal and posterior This increase is more wide-spread in the General attention than in the Selective attention task.…”

“…Several methods such as beamformers (Gross et al 2001), low resolution electromagnetic tomography (LORETA) (Pascual-Marqui et al 2011), and minimumnorm estimation (MNE) (Hamalainen and Ilmoniemi 1994;Lin et al 2006) have been developed for source reconstruction. Indeed, a large body of source reconstruction-based MEG studies have shown that the amplitudes of local cortical oscillations, which reflect synchronization in the local neuronal populations, are correlated with attention (Händel et al 2011;Rouhinen et al 2013;Zumer et al 2014), perception (Haegens et al 2011;Hirvonen and Palva 2016), and WM (Bonnefond and Jensen 2012;Honkanen et al 2015;Palva et al 2011;Roux et al 2012) and hence with many distinct cognitive functions.…”

“…Real WM capacity is displayed in x-axis and that predicted by oscillation amplitudes in the y-axis. Modified from refs (Palva et al 2011;Rouhinen et al 2013) parietal areas that are known to coordinate attention to sensory objects (Corbetta and Shulman 2002;Kastner and Ungerleider 2000) (Fig. 2b).…”

Magnetoencephalography in the study of brain dynamics

“…Oscillatory brain activity and its modulation have also been linked to visual attention. In particular, site-specific gamma oscillations have been linked to the individual's attention capacity, whereas suppression of theta to beta amplitudes has been correlated with attentional load (Rouhinen et al, 2013). In addition to the visual modality, auditory attention has been shown to modulate alpha power in auditory regions, and specifically in relation to the information content of the auditory cue (Weisz et al, 2014).…”