Principles of Corticocortical Communication: Proposed Schemes and Design Considerations

Kohn, Adam; Jasper, Anna I.; Semedo, João D.; Gokcen, Evren; Machens, Christian K.; Yu, Byron M.

doi:10.1016/j.tins.2020.07.001

Cited by 86 publications

(81 citation statements)

References 111 publications

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“…Our findings suggest that inhibitory subnetworks that are selectively activated by WM play a dual role in influencing excitatory cells, modulating both the sensory gain and phase locking to network oscillations. These WMmediated changes underly two principal hypotheses for topdown control of interareal cortical communication (Diesmann et al, 1999;Womelsdorf et al, 2007;Kumar et al, 2008;Fries, 2015;Moldakarimov et al, 2015;Kanashiro et al, 2017;Hahn et al, 2019;Kohn et al, 2020), where both spike count, as well as the degree of spike synchronization within an oscillation cycle, each contribute to communication efficacy.…”

Section: Introductionmentioning

confidence: 99%

Differential Contributions of Inhibitory Subnetwork to Visual Cortical Modulations Identified via Computational Model of Working Memory

Nesse

Bahmani

Clark

et al. 2021

Front. Comput. Neurosci.

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Extrastriate visual neurons show no firing rate change during a working memory (WM) task in the absence of sensory input, but both αβ oscillations and spike phase locking are enhanced, as is the gain of sensory responses. This lack of change in firing rate is at odds with many models of WM, or attentional modulation of sensory networks. In this article we devised a computational model in which this constellation of results can be accounted for via selective activation of inhibitory subnetworks by a top-down working memory signal. We confirmed the model prediction of selective inhibitory activation by segmenting cells in the experimental neural data into putative excitatory and inhibitory cells. We further found that this inhibitory activation plays a dual role in influencing excitatory cells: it both modulates the inhibitory tone of the network, which underlies the enhanced sensory gain, and also produces strong spike-phase entrainment to emergent network oscillations. Using a phase oscillator model we were able to show that inhibitory tone is principally modulated through inhibitory network gain saturation, while the phase-dependent efficacy of inhibitory currents drives the phase locking modulation. The dual contributions of the inhibitory subnetwork to oscillatory and non-oscillatory modulations of neural activity provides two distinct ways for WM to recruit sensory areas, and has relevance to theories of cortical communication.

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Section: Introductionmentioning

confidence: 99%

Differential Contributions of Inhibitory Subnetwork to Visual Cortical Modulations Identified via Computational Model of Working Memory

Nesse

Bahmani

Clark

et al. 2021

Front. Comput. Neurosci.

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“…To understand inter-areal interactions more deeply, it is now possible to record activity from large neuronal populations simultaneously in different cortical areas, and characterize what patterns of population activity are most related across those areas 19, 26-33 . This approach has led to new proposals about how activity can be flexibly routed across brain areas (see ref. 34 for a review). In particular, simultaneous multi-area recordings have revealed properties of population activity patterns that are most related across areas in the context of sensory processing 29 , attention 30 , learning 31 , and motor control 32,33 .…”

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confidence: 99%

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

Semedo

Jasper

Zandvakili

et al. 2021

Preprint

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Brain function relies on the coordination of activity across multiple, recurrently connected, brain areas. For instance, sensory information encoded in early sensory areas is relayed to, and further processed by, higher cortical areas and then fed back. However, the way in which feedforward and feedback signaling interact with one another is incompletely understood. Here we investigate this question by leveraging simultaneous neuronal population recordings in early and midlevel visual areas (V1-V2 and V1-V4). Using a dimensionality reduction approach, we find that population interactions are feedforward-dominated shortly after stimulus onset and feedback-dominated during spontaneous activity. The population activity patterns most correlated across areas were distinct during feedforward- and feedback-dominated periods. These results suggest that feedforward and feedback signaling rely on separate "channels", such that feedback signaling does not directly affect activity that is fed forward.

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“…However, new techniques will be required to better explore how inputs are processed by MC. Recent methods that exploit simultaneous recordings from multiple brain areas provide a promising tool to identify input signals to a given circuit (Kohn et al, 2020; Perich et al, 2018; Semedo et al, 2019). Using these techniques, Perich et al, (2020) provides evidence of a communication subspace between the somatosensory and motor cortices that contributes to a substantial amount of the variance in MC, consistent with inputs playing a key role in motor cortical dynamics.…”

Section: Discussionmentioning

confidence: 99%

Rotational dynamics in motor cortex are consistent with a feedback controller

Kalidindi

Cross

Lillicrap

et al. 2020

Preprint

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SummaryRecent studies hypothesize that motor cortical (MC) dynamics are generated largely through its recurrent connections based on observations that MC activity exhibits rotational structure. However, behavioural and neurophysiological studies suggest that MC behaves like a feedback controller where continuous sensory feedback and interactions with other brain areas contribute substantially to MC processing. We investigated these apparently conflicting theories by building recurrent neural networks that controlled a model arm and received sensory feedback about the limb. Networks were trained to counteract perturbations to the limb and to reach towards spatial targets. Network activities and sensory feedback signals to the network exhibited rotational structure even when the recurrent connections were removed. Furthermore, neural recordings in monkeys performing similar tasks also exhibited rotational structure not only in MC but also in somatosensory cortex. Our results argue that rotational structure may reflect dynamics throughout voluntary motor circuits involved in online control of motor actions.HighlightsNeural networks with sensory feedback generate rotational dynamics during simulated posture and reaching tasksRotational dynamics are observed even without recurrent connections in the networkSimilar dynamics are observed not only in motor cortex, but also in somatosensory cortex of non-huma n primates as well as sensory feedback signalsResults highlight rotational dynamics may reflect internal dynamics, external inputs or any combination of the two.

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Principles of Corticocortical Communication: Proposed Schemes and Design Considerations

Cited by 86 publications

References 111 publications

Differential Contributions of Inhibitory Subnetwork to Visual Cortical Modulations Identified via Computational Model of Working Memory

Differential Contributions of Inhibitory Subnetwork to Visual Cortical Modulations Identified via Computational Model of Working Memory

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

Rotational dynamics in motor cortex are consistent with a feedback controller

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