Top-down control of visual cortex by the frontal eye fields through oscillatory realignment

Veniero, Domenica; Groß, Joachim; Morand, S.; Duecker, Felix; Sack, Alexander T.; Thut, Gregor

doi:10.1038/s41467-021-21979-7

Cited by 76 publications

(68 citation statements)

References 69 publications

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“…There was no re-referencing as the region of interest was the occipital cortex. The spike artifact caused by a TMS pulse typically lasted 4–10 ms. To reduce the artifact, signals within 1 ms before and 13 ms after each TMS pulse were replaced with shape-preserving piecewise cubic interpolated data (MATLAB command: interp1 with ‘pchip’ option) 43 , 48 , 57 , 87 . The exact same procedure was applied to EEG data during sham auditory pulses to ensure that any statistical differences could not be attributed to discrepancies in data processing.…”

Section: Methodsmentioning

confidence: 99%

Transcranial magnetic stimulation entrains alpha oscillatory activity in occipital cortex

Lin

Shukla

Dugué

et al. 2021

Sci Rep

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Parieto-occipital alpha rhythms (8–12 Hz) underlie cortical excitability and influence visual performance. Whether the synchrony of intrinsic alpha rhythms in the occipital cortex can be entrained by transcranial magnetic stimulation (TMS) is an open question. We applied 4-pulse, 10-Hz rhythmic TMS to entrain intrinsic alpha oscillators targeting right V1/V2, and tested four predictions with concurrent electroencephalogram (EEG): (1) progressive enhancement of entrainment across time windows, (2) output frequency specificity, (3) dependence on the intrinsic oscillation phase, and (4) input frequency specificity to individual alpha frequency (IAF) in the neural signatures. Two control conditions with an equal number of pulses and duration were arrhythmic-active and rhythmic-sham stimulation. The results confirmed the first three predictions. Rhythmic TMS bursts significantly entrained local neural activity. Near the stimulation site, evoked oscillation amplitude and inter-trial phase coherence (ITPC) were increased for 2 and 3 cycles, respectively, after the last TMS pulse. Critically, ITPC following entrainment positively correlated with IAF rather than with the degree of similarity between IAF and the input frequency (10 Hz). Thus, we entrained alpha-band activity in occipital cortex for ~ 3 cycles (~ 300 ms), and IAF predicts the strength of entrained occipital alpha phase synchrony indexed by ITPC.

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Section: Methodsmentioning

confidence: 99%

Transcranial magnetic stimulation entrains alpha oscillatory activity in occipital cortex

Lin

Shukla

Dugué

et al. 2021

Sci Rep

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“…While this proposal may seem excessively radical in the extent to which embodiment is emphasized, convergent support can be found in substantial evidence implicating the “formation of internal motor traces” in working memory [ 124 ]. Further evidence may be obtained in attentional selection being enhanced when neuronal oscillations from frontal eye fields entrain sensory cortices [ 125 ], as well as from visual attention and working memory heavily depending on frontal-parietal networks [ 126 , 127 ] (which are here interpreted as upper levels of action-perception hierarchies). With respect to embodied sources of top-down attention, striatum and midbrain value signals (e.g., dopamine) likely play key roles [ 128 ], both influencing moment-to-moment pattern selection, and also allowing future planning to be influenced by histories of reinforcement and punishment.…”

Section: From Action To Attention and Back Againmentioning

confidence: 99%

“…Based on the models described above, these executive resources would heavily depend on networks utilized for simulating actions of varying degrees of complexity, with fictitious foveations and virtual motoric manipulations likely being especially impactful ( Table 2 ). Dorsomedial and dorsolateral prefrontal cortices provide higher-order control over frontal eye fields and pre-supplementary motor areas [ 74 ] ( Figure 6 ), which have both been associated with attention and working memory [ 125 , 294 , 295 ]. Strong evidence for these models would be obtained if executive failure (and recovery) were reliably indexed by local increases (and subsequent decreases with rest) in slow oscillations, as well as if stimulation [ 296 ] applied to these areas—or perhaps other integrative networks [ 297 ]—was found to increase self-control and promote repletion during rest intervals.…”

Section: The Emergence Of Conscious Teleological Agentsmentioning

confidence: 99%

The Radically Embodied Conscious Cybernetic Bayesian Brain: From Free Energy to Free Will and Back Again

Safron

2021

Entropy

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Drawing from both enactivist and cognitivist perspectives on mind, I propose that explaining teleological phenomena may require reappraising both “Cartesian theaters” and mental homunculi in terms of embodied self-models (ESMs), understood as body maps with agentic properties, functioning as predictive-memory systems and cybernetic controllers. Quasi-homuncular ESMs are suggested to constitute a major organizing principle for neural architectures due to their initial and ongoing significance for solutions to inference problems in cognitive (and affective) development. Embodied experiences provide foundational lessons in learning curriculums in which agents explore increasingly challenging problem spaces, so answering an unresolved question in Bayesian cognitive science: what are biologically plausible mechanisms for equipping learners with sufficiently powerful inductive biases to adequately constrain inference spaces? Drawing on models from neurophysiology, psychology, and developmental robotics, I describe how embodiment provides fundamental sources of empirical priors (as reliably learnable posterior expectations). If ESMs play this kind of foundational role in cognitive development, then bidirectional linkages will be found between all sensory modalities and frontal-parietal control hierarchies, so infusing all senses with somatic-motoric properties, thereby structuring all perception by relevant affordances, so solving frame problems for embodied agents. Drawing upon the Free Energy Principle and Active Inference framework, I describe a particular mechanism for intentional action selection via consciously imagined (and explicitly represented) goal realization, where contrasts between desired and present states influence ongoing policy selection via predictive coding mechanisms and backward-chained imaginings (as self-realizing predictions). This embodied developmental legacy suggests a mechanism by which imaginings can be intentionally shaped by (internalized) partially-expressed motor acts, so providing means of agentic control for attention, working memory, imagination, and behavior. I further describe the nature(s) of mental causation and self-control, and also provide an account of readiness potentials in Libet paradigms wherein conscious intentions shape causal streams leading to enaction. Finally, I provide neurophenomenological handlings of prototypical qualia including pleasure, pain, and desire in terms of self-annihilating free energy gradients via quasi-synesthetic interoceptive active inference. In brief, this manuscript is intended to illustrate how radically embodied minds may create foundations for intelligence (as capacity for learning and inference), consciousness (as somatically-grounded self-world modeling), and will (as deployment of predictive models for enacting valued goals).

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“…On a theoretical level, such phase resets may reflect alignment of sensory and motor systems for the sensorimotor sampling process described across many different species (Schroeder et al, 2010). Indeed, eye-movement related top-down signals appear to affect both perception and the phase of neural oscillations (Veniero et al, 2021). Other studies have investigated the relationship between alpha oscillations and saccades (Drewes and VanRullen, 2011;Staudigl et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

Changes in neural activity around the time of saccades: Separate contributions of visual and non-visual signals on MEG alpha and theta band activity

Acunzo¹,

Melcher²

2021

Preprint

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Visual processing mainly occurs during fixation, periods separated by saccadic eye movements, necessitating a close coordination between sensory and motor systems. It has been suggested that the intention to make a saccade can modulate neural activity, including predictive changes, suppression of peri-saccadic retinal input and trans-saccadic integration. Consistent with this idea, modulations of neural activity around the time of saccades have been reported in non-human species, showing non-visually mediated, extraretinal responses in specific brain regions. In humans, however, peri-saccadic whole-brain activity has mainly been studied in the context of a perceptual task, making it difficult to disentangle activity related to the task, visual transients from retinal stimulation and non-visual (saccade-related) responses. We measured magnetoencephalography (MEG) theta (3–7 Hz) and alpha (8–12 Hz) activity during voluntary horizontal saccade execution between two fixation points. To distinguish between visually and non-visually mediated activity, participants engaged in three tasks: voluntary saccades in near-darkness, fixation with visual input shifted to simulate the saccade, and volitional saccades in total darkness. Using correlational analyses, we found that patterns of neural activity are consistent with contributions of two separate mechanisms, one related to saccades (non-visual/extraretinal) and the other linked to the processing of visual input at the beginning of the new fixation (visual/retinal). Changes in occipital alpha power and instantaneous frequency showed a similar time course in near-dark and simulated saccade conditions, suggesting an effect of visually evoked responses. In contrast, alterations in parietal-occipital theta power and phase clustering were consistent with a non-visually-driven (extraretinal) mechanism, with similar multivariate patterns for near-dark and full-darkness conditions. Some effects, such as theta phase reset and alterations in alpha power, showed separable contributions of both the saccade and visual transient, with differing time courses. This combination of visual and non-visual mechanisms may support sensorimotor integration during active vision.

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Top-down control of visual cortex by the frontal eye fields through oscillatory realignment

Cited by 76 publications

References 69 publications

Transcranial magnetic stimulation entrains alpha oscillatory activity in occipital cortex

Transcranial magnetic stimulation entrains alpha oscillatory activity in occipital cortex

The Radically Embodied Conscious Cybernetic Bayesian Brain: From Free Energy to Free Will and Back Again

Changes in neural activity around the time of saccades: Separate contributions of visual and non-visual signals on MEG alpha and theta band activity

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