Inferring Thalamocortical Monosynaptic Connectivity In-Vivo

Liew, Yi Juin; Pala, Aurélie; Whitmire, Clarissa J.; Stoy, William; Forest, Craig R.; Stanley, Garrett B.

doi:10.1101/2020.10.09.333930

Cited by 4 publications

(7 citation statements)

References 85 publications

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“…We used a precise, computer-controlled galvanometer (Cambridge Technologies) with attached tube to stimulate individual whiskers (Whitmire et al, 2016; Waiblinger et al, 2018; Sederberg et al, 2019; Liew et al, 2020). The galvanometer was controlled using either a custom Matlab GUI and Simulink Real-Time (MathWorks), or the Real-time eXperiment Interface application (http://rtxi.org/), sampling at 1 kHz.…”

Section: Methodsmentioning

confidence: 99%

Rapid Cortical Adaptation and the Role of Thalamic Synchrony During Wakefulness

Borden

Liew

et al. 2020

Preprint

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Rapid sensory adaptation is observed across all sensory systems, and strongly shapes sensory percepts in complex sensory environments. Yet despite its ubiquity and likely necessity for survival, the mechanistic basis is poorly understood. A wide range of studies primarily in in-vitro and anesthetized preparations have pointed to the emergence of adaptation effects at the level of primary sensory cortex, with only modest signatures in earlier stages of processing. The nature of rapid adaptation and how it shapes sensory representations during wakefulness, and thus the potential role in adaptive changes in perception, is unknown, as are the mechanisms that underlie this phenomenon. To address these unknowns, we recorded spiking activity in primary somatosensory cortex (S1) and the upstream ventral posteromedial (VPm) thalamic nucleus in the vibrissa pathway of the awake mouse, and quantified responses to whisker stimuli delivered in isolation and embedded in an adapting sensory background. We found that during wakefulness, cortical sensory responses were indeed adapted by persistent sensory stimulation; putative excitatory neurons were profoundly adapted, and inhibitory neurons only modestly so. Further optogenetic manipulation experiments and network modeling suggest this largely reflects adaptive changes in synchronous thalamic firing combined with robust engagement of feedforward inhibition, with little contribution from synaptic depression. Taken together, these results suggest that cortical adaptation largely reflects changes in timing of thalamic input, and the way in which this differentially impacts cortical excitation and feedforward inhibition, pointing to a prominent role of thalamic gating in rapid adaptation of primary sensory cortex.Significance StatementRapid adaptation of sensory activity strongly shapes representations of sensory inputs across all sensory pathways over the timescale of seconds, and has profound effects on sensory perception. Despite its ubiquity and theoretical role in the efficient encoding of complex sensory environments, the mechanistic basis is poorly understood, particularly during wakefulness. In this study in the vibrissa pathway of awake mice, we show that cortical representations of sensory inputs are strongly shaped by rapid adaptation, and that this is mediated primarily by adaptive gating of the thalamic inputs to primary sensory cortex and the differential way in which these inputs engage cortical sub-populations of neurons.

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Section: Methodsmentioning

confidence: 99%

Rapid Cortical Adaptation and the Role of Thalamic Synchrony During Wakefulness

Borden

Liew

et al. 2020

Preprint

Self Cite

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“…We used a precise, computer-controlled galvanometer (Cambridge Technologies) with attached tube to stimulate individual whiskers Waiblinger et al, 2018;Sederberg et al, 2019;Liew et al, 2020). The galvanometer was controlled using either a custom MATLAB GUI and Simulink Real-Time (MathWorks), or the Realtime eXperiment Interface application (http://rtxi.org/), sampling at 1 kHz.…”

Section: Whisker Stimulationmentioning

confidence: 99%

Rapid Cortical Adaptation and the Role of Thalamic Synchrony during Wakefulness

Borden

Liew

et al. 2021

J. Neurosci.

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Rapid sensory adaptation is observed across all sensory systems, and strongly shapes sensory percepts in complex sensory environments. Yet despite its ubiquity and likely necessity for survival, the mechanistic basis is poorly understood. A wide range of primarily in vitro and anesthetized studies have demonstrated the emergence of adaptation at the level of primary sensory cortex, with only modest signatures in earlier stages of processing. The nature of rapid adaptation and how it shapes sensory representations during wakefulness, and thus the potential role in perceptual adaptation, is underexplored, as are the mechanisms that underlie this phenomenon. To address these knowledge gaps, we recorded spiking activity in primary somatosensory cortex (S1) and the upstream ventral posteromedial (VPm) thalamic nucleus in the vibrissa pathway of awake male and female mice, and quantified responses to whisker stimuli delivered in isolation and embedded in an adapting sensory background. We found that cortical sensory responses were indeed adapted by persistent sensory stimulation; putative excitatory neurons were profoundly adapted, and inhibitory neurons only modestly so. Further optogenetic manipulation experiments and network modeling suggest this largely reflects adaptive changes in synchronous thalamic firing combined with robust engagement of feedforward inhibition, with little contribution from synaptic depression. Taken together, these results suggest that cortical adaptation in the regime explored here results from changes in the timing of thalamic input, and the way in which this differentially impacts cortical excitation and feedforward inhibition, pointing to a prominent role of thalamic gating in rapid adaptation of primary sensory cortex.

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“…The thalamus provides the main afferent input to all cortical regions and is crucial for its computations 1– 6 and its functional organization 2,7 . However, how spikes from thalamic neurons are integrated into the ongoing cortical activity in behaving animals remains largely unknown due to technical difficulties in recording synaptically connected thalamocortical neuron pairs in vivo 8 . Electrophysiological paired recordings are the gold standard for characterizing monosynaptic connectivity in vivo 1,3,6,9 .…”

Section: Mainmentioning

confidence: 99%

“…However, in vivo paired recordings require a precise alignment between the electrodes in the thalamus and cortex to capture the activity of synaptically connected thalamocortical neuron pairs. This step is technically challenging and therefore limiting the numbers of identified connected neuron pairs per experiment 8 . Consequently, while important progress has been made over the last decades 1– 6,8,10 , our overall understanding of the thalamocortical processing in sensory and non-sensory areas remains incomplete and is an active field of research 11 .…”

Section: Mainmentioning

confidence: 99%

“…This step is technically challenging and therefore limiting the numbers of identified connected neuron pairs per experiment 8 . Consequently, while important progress has been made over the last decades [1][2][3][4][5][6]8,10 , our overall understanding of the thalamocortical processing in sensory and non-sensory areas remains incomplete and is an active field of research 11 .A method capable of reliably recording the activity of synaptically connected thalamic and cortical neurons in vivo would greatly advance our understanding of thalamocortical processing and could reveal the mechanisms underlying perception and behavior. Recording the activity of thalamic neurons at the axonal level within cortex, simultaneously with the activity of nearby cortical neurons, would overcome the challenging step of aligning multiple probes across distant brain regions and allow to map the thalamocortical connectivity in a more efficient manner.…”

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confidence: 99%

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Efficient mapping of the thalamocortical monosynaptic connectivityin vivoby tangential insertions of high-density electrodes in cortex

Sibille

Gehr

Kremkow

2022

Preprint

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Thalamus provides the principal input to cortex, thus understanding the mechanisms of cortical computations in behaving animals requires to characterize the thalamocortical connectivity in vivo. We show that tangential insertions of high-density electrodes into mouse cortex capture the activity of thalamocortical axons simultaneously with their synaptically connected cortical neurons. Multiple thalamic synaptic inputs to cortical neurons can be measured providing an efficient approach for mapping the thalamocortical connectivity in vivo.

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Inferring Thalamocortical Monosynaptic Connectivity In-Vivo

Cited by 4 publications

References 85 publications

Rapid Cortical Adaptation and the Role of Thalamic Synchrony During Wakefulness

Rapid Cortical Adaptation and the Role of Thalamic Synchrony During Wakefulness

Rapid Cortical Adaptation and the Role of Thalamic Synchrony during Wakefulness

Efficient mapping of the thalamocortical monosynaptic connectivityin vivoby tangential insertions of high-density electrodes in cortex

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