Visual areas exert feedforward and feedback influences through distinct frequency channels
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Abstract
Visual cortical areas subserve cognitive functions by interacting in both feedforward and feedback directions. While feedforward influences convey sensory signals, feedback influences modulate feedforward signaling according to the current behavioral context. We investigated whether these interareal influences are subserved differentially by rhythmic synchronization. We correlated frequency-specific directed influences among 28 pairs of visual areas with anatomical metrics of the feedforward or feedback character of the respective interareal projections. This revealed that in the primate visual system, feedforward influences are carried by theta-band (∼ 4 Hz) and gamma-band (∼ 60-80 Hz) synchronization, and feedback influences by beta-band (∼ 14-18 Hz) synchronization. The functional directed influences constrain a functional hierarchy similar to the anatomical hierarchy, but exhibiting task-dependent dynamic changes in particular with regard to the hierarchical positions of frontal areas. Our results demonstrate that feedforward and feedback signaling use distinct frequency channels, suggesting that they subserve differential communication requirements.
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Adding layer-specific connectivity to simulations produces frequency-band-specific causality patterns-bottom-up gamma from supragranular layers and top-down alpha-beta from bottom layers-which have been observed empirically across the cortical hierarchy in humans and non-human primates.
“Addition of layer-specific connectivity in simulations (Mejias et al., 2016) leads to the emergence of frequency-band-specific patterns of causality (bottom-up gamma arising primarily in supragranular layers versus top-down alpha-beta arising primarily from bottom layers)”
From Conscious Processing and the Global Neuronal Workspace Hypothesis (2020) · cites this paper as Bastos et al., 2015
Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measuredEvidence from monkey and human studies indicates that gamma-band activity predominantly emanates from forward projections in superficial layers.
“Consistent with the proposed laminar profile of PP dynamics, evidence from monkey and human studies indicate that gamma‐band activity predominantly emanates from forward projections in superficial layers, while descending activity, carried by alpha/beta‐band activity, is strongest in layers 5/6.”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [170]
The Discussion (p. 7) reports that gamma-band communication is feedforward and that gamma synchronization predominates in superficial layers. But the Results (p. 3) describe recordings from two macaque monkeys, not humans, and the Discussion says the proposed link between frequency-specific influences and cortical layers still needs direct testing. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn the primate visual system, backward signaling is carried out through beta-band activity (12-30 Hz).
“In the primate visual system, signals transmitted forward through hierarchical levels are expressed in theta‐band (4–8 Hz) and gamma‐band (>30 Hz) activity, while backward signaling is carried out through beta‐band activity (12–30 Hz).”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [170]
The Discussion (p. 7) states that feedback communication among primate visual cortical areas uses the beta band. The specified 12–30 Hz range does not match the bands defined for the two monkeys in Data Analysis General (p. 11): 12–24 Hz and 7–21 Hz. (LLM, conf=0.86)
Experimental — accuracy not yet measuredIn the primate visual system, signals transmitted forward through hierarchical levels are expressed in theta-band (4-8 Hz) and gamma-band (>30 Hz) activity.
“In the primate visual system, signals transmitted forward through hierarchical levels are expressed in theta‐band (4–8 Hz) and gamma‐band (>30 Hz) activity, while backward signaling is carried out through beta‐band activity (12–30 Hz).”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [170]
The Summary (p. 2) and Discussion (p. 7) support the central claim that feedforward influences in primate visual areas use theta- and gamma-band activity. The stated theta range does not match the study’s definition: Data Analysis General (p. 11) defines theta as 2–6 Hz in both monkeys, not 4–8 Hz. The measured gamma bands fall above 30 Hz. (LLM, conf=0.86)
Experimental — accuracy not yet measuredGamma power/spiking is anticorrelated with alpha/beta (8 to 30 Hz) power, which is higher under conditions of top-down control (e.g., attention and response inhibition).
“They are anticorrelated with alpha/beta (8 to 30 Hz) power (26–29), which is higher under conditions of top-down control (e.g., attention and response inhibition) (30–34).”
From Layer and rhythm specificity for predictive routing (2020) · cites this paper as [30]
The section “Attention Enhances Top-Down and Bottom-up Influences in a Spatially Specific Manner” (p. 7) reports stronger top-down beta-band Granger-causal influences with selective attention, supporting the attention example. It measures directed influences rather than alpha/beta power, and the cited passages do not establish the response-inhibition example or an anticorrelation with gamma power or spiking. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Electrocorticography during propofol and ketamine anesthesia in human and non-human primates reveals disrupted functional connectivity across S1 and M1 cortex, as well as altered beta oscillations typically associated with feedback processing.
“Electrocorticography during propofol (Malekmohammadi et al., 2018) and ketamine (Schroeder et al., 2016) anesthesia in human and non-human primates, respectively, reveals disrupted functional connectivity across the S1 and M1 cortex, as well as altered beta oscillations, which are typically associated with feedback processing (Bastos et al., 2015).”
From Conscious Processing and the Global Neuronal Workspace Hypothesis (2020) · cites this paper as Bastos et al., 2015
Descending activity, carried by alpha/beta-band activity, is strongest in layers 5/6.
“Consistent with the proposed laminar profile of PP dynamics, evidence from monkey and human studies indicate that gamma‐band activity predominantly emanates from forward projections in superficial layers, while descending activity, carried by alpha/beta‐band activity, is strongest in layers 5/6.”
From Evaluating the neurophysiological evidence for predictive processing as a model of perception (2020) · cites this paper as [170]
Oscillatory signals have been related to predictive coding, with feedback signaling of predictions mediated predominantly by alpha/beta frequency bands and feedforward prediction error signaling by gamma-band activity.
“In the time-frequency domain, oscillatory signals have been related to predictive coding, with feedback signaling of predictions being mediated predominantly by the alpha/beta frequency bands and feedforward PE signaling by gamma-band activity (14, 35–37).”
From The Predictive Coding Account of Psychosis (2018) · cites this paper as [37]
Frontoparietal cortex has a well-established role in top-down attention and working memory, cognitive processes engaged in the task employed here.
“Frontoparietal cortex was targeted because of its well-established role in top-down attention and working memory, cognitive processes that are engaged in the task employed here (30, 31).”
From Layer and rhythm specificity for predictive routing (2020) · cites this paper as [30]
A previous study identified theta as a carrier for feedforward interactions in the visual system.
“In addition, a previous study identified theta as a carrier for feedforward interactions in the visual system (30).”
From Layer and rhythm specificity for predictive routing (2020) · cites this paper as [30]
Recent studies suggest that low-frequency oscillations (e.g., alpha) reflect feedback and high-frequency oscillations (e.g., gamma) reflect feedforward network interactions.
“Recent studies suggest that the frequency of neural oscillations marks the directionality of network interactions: low-frequency oscillations (e.g. alpha) reflect feedback processes and high-frequency oscillations (e.g. gamma) reflect feedforward processes (184–186).”
From Electrophysiological source imaging: A noninvasive window to brain dynamics (2018) · cites this paper as [185]
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- Authors
- Bastos, A. M., Vezoli, J., Bosman, C. A., Schoffelen, J.-M., Oostenveld, R., Dowdall, J. R., De Weerd, P., Kennedy, H., & Fries, P.
- Affiliations
- Radboud University Nijmegen (NL)
- Max Planck Society (DE)
- Inserm (FR)
- Corresponding author
- Fries, Pascal
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2015-01
- Volume
- 85
- Issue
- 2
- Pages
- 390-401
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2096629297
- Cited by
- 1,320
- References
- 55
- Citations by year
- 2026: 104 · 2025: 113 · 2024: 130 · 2023: 120 · 2022: 116 · 2021: 119 · 2020: 121 · 2019: 112 · 2018: 126 · 2017: 92 · 2016: 100 · 2015: 57 · 2014: 9
- FWCI
- 47.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- UvA-DARE (University of Amsterdam) (publishedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Research Publications (Maastricht University) (submittedVersion, other-oa)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Funders
- National Science Foundation (2009090358)
- U.S. Department of State
- European Commission (200728)
- European Science Foundation
- Volkswagen Foundation (I/79876)
- Agence Nationale de la Recherche (ANR-11-BSV4-501, ANR-14-CE13-0033, ANR-15-CE32-0016, ANR-11-LABX-0042)
- Ministerie van Economische Zaken
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- visual cortex, rhythm synchronization, theta band, gamma band, beta band, functional hierarchy, frontal area, primate visual system
- MeSH terms
- Animals, Beta Rhythm, Electroencephalography, Macaca mulatta, Male, Photic Stimulation, Theta Rhythm, Visual Cortex, Feedback, Physiological, Gamma Rhythm
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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