Feedforward and feedback interactions between visual cortical areas use different population activity patterns

Semedo, João D.; Jasper, Anna I.; Zandvakili, Amin; Krishna, Aravind; Aschner, Amir; Machens, Christian K.; Kohn, Adam; Yu, Byron M.

doi:10.1038/s41467-022-28552-w

Cited by 75 publications

(58 citation statements)

References 72 publications

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“…In our previous studies, we explored the direction of information flow within the circuitry of areas 3b and 1 (Wang et al, 2013;Pálfi et al, 2018). The picture that emerged from that data is consistent with the findings of Polack and Contreras (2012) who found that in the mouse visual cortex information is rapidly forwarded to numerous cortical areas, simultaneously triggering slower serial processing within areas, which can be influenced by the later feedback component in population activity (Semedo et al, 2022). Patchy organization is a characteristic feature of the wiring motif of the mesoscale network of the cerebral cortex of higher order mammals (Roe, 2019).…”

Section: Functional Considerationssupporting

confidence: 74%

Modular Organization of Signal Transmission in Primate Somatosensory Cortex

et al. 2022

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Axonal patches are known as the major sites of synaptic connections in the cerebral cortex of higher order mammals. However, the functional role of these patches is highly debated. Patches are formed by populations of nearby neurons in a topographic manner and are recognized as the termination fields of long-distance lateral connections within and between cortical areas. In addition, axons form numerous boutons that lie outside the patches, whose function is also unknown. To better understand the functional roles of these two distinct populations of boutons, we compared individual and collective morphological features of axons within and outside the patches of intra-areal, feedforward, and feedback pathways by way of tract tracing in the somatosensory cortex of New World monkeys. We found that, with the exception of tortuosity, which is an invariant property, bouton spacing and axonal convergence properties differ significantly between axons within patch and no-patch domains. Principal component analyses corroborated the clustering of axons according to patch formation without any additional effect by the type of pathway or laminar distribution. Stepwise logistic regression identified convergence and bouton density as the best predictors of patch formation. These findings support that patches are specific sites of axonal convergence that promote the synchronous activity of neuronal populations. On the other hand, no-patch domains could form a neuroanatomical substrate to diversify the responses of cortical neurons.

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Section: Functional Considerationssupporting

confidence: 74%

Modular Organization of Signal Transmission in Primate Somatosensory Cortex

et al. 2022

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“…However, analyses of population dynamics do not allow a direct estimate of computation. Historically, the amount of information processed was either estimated based on correlation analyses [48] or indirectly inferred via an artificial neural network model [49]. Prior work on the inference of network connectivity at the neuron-level has demonstrated the presence of strong inter- and intra-are connectivity and an area spanning rich-club of neurons [28], but its behavioral relevance was elusive.…”

Section: Discussionmentioning

confidence: 99%

Information processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior

Varley

Sporns

Scherberger

et al. 2021

Preprint

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The brain is often described as "processing" information: somehow, the decentralized interactions of billions of neurons collectively are somehow able to give rise to "emergent" behaviors, such as perception, cognition, and action. In neuroscience and cognitive science, however, "information processing" is often vaguely defined, making an exact model connecting neurodynamics, information processing, and behavior difficult to pin down. While considerable previous work has examined the structure of information dynamics in cultures or models, it remains uncertain what insights information dynamics can provide about cognition and behavior in order to interact with the environment. In this paper, we use information theory and the theory of information dynamics as a formal framework to explore information processing in multi area neuronal networks recorded from three macaques engaged in sensory-motor transformations: perceiving a visual cue, preparation of a grasping movement, and movement execution. We found that different states and grasp conditions are associated with significant re-configurations of the effective network structure and the overall information flowing through the system. Crucially, differences between cognitive and behavioral states and conditions were related to changes to higher-order, synergistic information dynamics not localizable to a single pair of source/target neurons. Our results suggest that the combined application of information-theoretic analysis of dynamics and network science inference to networks of neurons is a powerful tool to probe the neuronal basis of cognition and behavior. Keywords: Information Theory, Macaque, Synergy, Transfer Entropy, Networks.

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“…Because this hypothesis is intuitive, it has long dominated research in the field despite lack of direct support. Previous studies have either demonstrated attention-related interactions between cortical areas without establishing causality (5,(36)(37)(38)(39) or used causal manipulations to perturb cortical feedback without measuring attentional signals (1,3,8,9,40). Furthermore, previous studies have largely ignored laminar-specific changes, although it is well accepted that feedback connections are layer-specific, and hence their effects on neuronal responses may vary across the targeted cortical column.…”

Section: Discussionmentioning

confidence: 99%

Suppressing feedback signals to visual cortex abolishes attentional modulation

Debes

Dragoi

2023

Science

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Attention improves perception by enhancing the neural encoding of sensory information. A long-standing hypothesis is that cortical feedback projections carry top-down signals to influence sensory coding. However, this hypothesis has never been tested to establish causal links. We used viral tools to label feedback connections from cortical area V4 targeting early visual cortex (area V1). While monkeys performed a visual–spatial attention task, inactivating feedback axonal terminals in V1 without altering local intracortical and feedforward inputs reduced the response gain of single cells and impaired the accuracy of neural populations for encoding external stimuli. These effects are primarily manifested in the superficial layers of V1 and propagate to downstream area V4. Attention enhances sensory coding across visual cortex by specifically altering the strength of corticocortical feedback in a layer-dependent manner.

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Feedforward and feedback interactions between visual cortical areas use different population activity patterns

Cited by 75 publications

References 72 publications

Modular Organization of Signal Transmission in Primate Somatosensory Cortex

Modular Organization of Signal Transmission in Primate Somatosensory Cortex

Information processing dynamics in neural networks of macaque cerebral cortex reflect cognitive state and behavior

Suppressing feedback signals to visual cortex abolishes attentional modulation

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