Causal frequency-specific contributions of frontal spatiotemporal patterns induced by non-invasive neurostimulation to human visual performance

Neural oscillatory activity is known to play a crucial role in brain function. In the particular domain of visual perception, specific frequency bands in different brain regions and networks, from sensory areas to large-scale frontoparietal systems, have been associated with distinct aspects of visual behavior. Nonetheless, their contributions to human visual cognition remain to be causally demonstrated. We hereby used non-uniform (and thus non-frequency-specific) and uniform (frequency-specific) high-beta and gamma patterns of noninvasive neurostimulation over the right frontal eye field (FEF) to isolate the behavioral effects of oscillation frequency and provide causal evidence that distinct visual behavioral outcomes could be modulated by frequency-specific activity emerging from a single cortical region. In a visual detection task using near-threshold targets, high-beta frequency enhanced perceptual sensitivity (d ) without changing response criterion (beta), whereas gamma frequency shifted response criterion but showed no effects on perceptual sensitivity. The lack of behavioral modulations by non-frequency-specific patterns demonstrates that these behavioral effects were specifically driven by burstfrequency. We hypothesizethat suchfrequency-coded behavioral impact of oscillatory activity may reflect a general brain mechanism to multiplex functions within the same neural substrate. Furthermore, pathological conditions involving impaired cerebral oscillations could potentially benefit in the near future from the use of neurostimulation to restore the characteristic oscillatory patterns of healthy systems

Contributions frontales et pariétales à la perception visuelle humaine

Les aires cérébrales frontales et pariétales sont impliquées dans différents processus cognitifs importants pour la performance visuelle, tels que l'attention ou la conscience. Malgré les preuves existantes en faveur d'une implication de ces régions dans la cognition visuelle, leurs contributions dans le traitement de stimuli non masqués de faible contraste ainsi que l'activité spatio-temporelle sous-tendant ces contributions restent largement inexplorées, tout particulièrement en termes de causalité. Nous avons mené une exploration approfondie de ces contributions chez l'humain, en mettant l'accent sur la dynamique de l'activité neurale et les améliorations perceptives potentielles qui peuvent résulter de la manipulation non invasive de l'activité cérébrale. À cette fin, nous avons testé chez des sujets sains les effets d'impulsions simples ou de rafales courtes de stimulation magnétique transcrânienne (SMT) réelle versus fausse, délivrée sur le champ oculomoteur frontal ou le sillon intrapariétal avant la présentation d'un filtre de Gabor de faible contraste, sur la discrimination et la détection consciente de ce filtre de Gabor. Nos résultats montrent que chez l'humain, la distribution spatio-temporelle de l'activité frontale et pariétale joue un rôle causal dans la performance visuelle. Nos recherches contribuent à mieux comprendre les bases oscillatoires de la cognition visuelle et les comportements associés et à préparer le terrain pour le développement de nouvelles thérapies basées sur la manipulation non-invasive de l'activité cérébrale oscillatoire avec, pour objectif ultime, l'amélioration des pathologies neuropsychiatriques.Frontal and parietal areas have been shown to subtend different cognitive processes such as attentional orienting, decision making and access to consciousness, with bearing on visual performance. In spite of prior evidence supporting an implication of those regions in visual cognition, their contributions to the processing of low-contrast unmasked stimuli and the characteristic spatiotemporal activity patterns underlying them remain to be fully explored and causation is lacking. We here addressed a thorough exploration of such contributions in humans, with an emphasis on the dynamics of neural activity and visual performance enhancements as probed by patterns of noninvasive manipulation of local brain oscillatory activity. To this end, we tested in healthy participants the effects of either single pulses or short bursts of active vs. sham transcranial magnetic stimulation (TMS), delivered to the frontal eye field (FEF) and the intraparietal sulcus (IPS) prior to the presentation of a lateralized low-contrast near-threshold Gabor stimulus, on the visual discrimination and conscious detection of such stimulus. Our findings contribute to better substantiate the oscillatory basis of visual cognition and its associated behaviors and to set the stage for the development of novel therapies based on noninvasive manipulation of dysfunctional brain oscillatory activity.PARIS-JUSSIEU-Bib.électronique (751059901) / SudocSudocFranceF

Fronto-parietal anatomical connections influence the modulation of conscious visual perception by high-beta frontal oscillatory activity

May white matter connectivity influence rhythmic brain activity underlying visual cognition? We here employed diffusion imaging to reconstruct the fronto-parietal white matter pathways in a group of healthy participants who displayed frequency-specific ameliorations of visual sensitivity during the entrainment of high-beta oscillatory activity by rhythmic transcranial magnetic stimulation over their right frontal eye field. Our analyses reveal a strong tract-specific association between the volume of the first branch of the superior longitudinal fasciculus and improvements of conscious visual detection driven by frontal beta oscillation patterns. These data indicate that the architecture of specific white matter pathways has the ability to influence the distributed effects of rhythmic spatio-temporal activity, and suggest a potentially relevant role for long-range connectivity in the synchronization of oscillatory patterns across fronto-parietal networks subtending the modulation of conscious visual perception

Cross-modal cueing effects of visuospatial attention on conscious somatosensory perception

The impact of visuospatial attention on perception with supraliminal stimuli and stimuli at the threshold of conscious perception has been previously investigated. In this study, we assess the cross-modal effects of visuospatial attention on conscious perception for near-threshold somatosensory stimuli applied to the face. Fifteen healthy participants completed two sessions of a near-threshold cross-modality cue-target discrimination/conscious detection paradigm. Each trial began with an endogenous visuospatial cue that predicted the location of a weak near-threshold electrical pulse delivered to the right or left cheek with high probability (75%). Participants then completed two tasks: first, a forced-choice somatosensory discrimination task (felt once or twice) and then, a somatosensory conscious detection task (did you feel the stimulus and, if yes, where (left/right)). Somatosensory discrimination was evaluated with the response reaction times of correctly detected targets, whereas the somatosensory conscious detection was quantified using perceptual sensitivity (d') and response bias (beta). A 2 × 2 repeated measures ANOVA was used for statistical analysis. In the somatosensory discrimination task (1st task), participants were significantly faster in responding to correctly detected targets (p < 0.001). In the somatosensory conscious detection task (2nd task), a significant effect of visuospatial attention on response bias (p = 0.008) was observed, suggesting that participants had a less strict criterion for stimuli preceded by spatially valid than invalid visuospatial cues. We showed that spatial attention has the potential to modulate the discrimination and the conscious detection of near-threshold somatosensory stimuli as measured, respectively, by a reduction of reaction times and a shift in response bias toward less conservative responses when the cue predicted stimulus location. A shift in response bias indicates possible effects of spatial attention on internal decision processes. The lack of significant results in perceptual sensitivity (d') could be due to weaker effects of endogenous attention on perception

Visual contrast sensitivity improvement by right frontal high-beta activity is mediated by contrast gain mechanisms and influenced by fronto-parietal white matter microstructure

Behavioral and electrophysiological studies in humans and non-human primates have correlated frontal high-beta activity with the orienting of endogenous attention and shown the ability of the latter function to modulate visual performance. We here combined rhythmic transcranial magnetic stimulation (TMS) and diffusion imaging to study the relation between frontal oscillatory activity and visual performance, and we associated these phenomena to a specific set of white matter pathways that in humans subtend attentional processes. High-beta rhythmic activity on the right frontal eye field (FEF) was induced with TMS and its causal effects on a contrast sensitivity function were recorded to explore its ability to improve visual detection performance across different stimulus contrast levels. Our results show that frequency-specific activity patterns engaged in the right FEF have the ability to induce a leftward shift of the psychometric function. This increase in visual performance across different levels of stimulus contrast is likely mediated by a contrast gain mechanism. Interestingly, microstructural measures of white matter connectivity suggest a strong implication of right fronto-parietal connectivity linking the FEF and the intraparietal sulcus in propagating high-beta rhythmic signals across brain networks and subtending top-down frontal influences on visual performance