Rapid Plasticity of Higher-Order Thalamocortical Inputs during Sensory Learning

Audette, Nicholas J.; Bernhard, Sarah; Ray, Ajit; Stewart, Luke T.; Barth, Alison L.

doi:10.1016/j.neuron.2019.04.037

Cited by 79 publications

(139 citation statements)

References 61 publications

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“…Here we use an automated, homecage system for sensory association training (SAT) to 74 examine the laminar location and trajectory of changes in PV-mediated inhibition in primary 75 somatosensory (barrel) cortex during learning. Our prior studies have shown that excitatory 76 synaptic strengthening sequentially progresses across the cortical column during SAT, starting 77 in deep layers and progressing to superficial layers (Audette et al, 2019). In accordance with 78 the disinhibition hypothesis (Letzkus et al, 2015) , we predicted that PV disinhibition would be 79 initiated in deep layers, where thalamic input potentiation is first observed, and would then 80 proceed to superficial layers prior to the emergence of excitatory strengthening there.…”

Section: Introduction 40supporting

confidence: 59%

“…Our prior studies indicate that SAT drives progressive changes in anticipatory licking and 95 excitatory synaptic strength that are initiated early in the training period (Audette et al, 2019). 96…”

Section: Prolonged Sensory Association Training Reveals Multiple Stagmentioning

confidence: 97%

“…Our prior studies showed that passive sensory stimulation in the absence of reward was 166 not sufficient to potentiate thalamocortical inputs to neocortical neurons (Audette et al, 2019). 167…”

Section: Passive Sensory Experience Alone Does Not Alter Pv Inhibitiomentioning

confidence: 99%

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Transient and layer-specific reduction in neocortical PV inhibition during sensory association learning

Kuljis

Park

Myal

et al. 2020

Preprint

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Sensory and motor learning reorganizes neocortical circuitry, particularly manifested in the strength of excitatory synapses. Prior studies suggest reduced inhibition can facilitate glutamatergic synapse plasticity during learning, but the role of specific inhibitory neurons in this process has not been well-documented. Here we investigate whether inhibition from parvalbumin (PV)-expressing neurons is altered in primary somatosensory cortex in mice trained in a whisker-based reward-association task. Anatomical and electrophysiological analyses show PV input to L2/3, but not L5, pyramidal (Pyr) neurons is rapidly suppressed during early stages of sensory training, effects that are reversed after longer training periods. Importantly, sensory stimulation without reward does not alter PV-mediated inhibition. Computational modeling indicates that reduced PV inhibition in L2/3 selectively enables an increase in translaminar recurrent activity, also observed during SAT. PV disinhibition in superficial layers of the neocortex may be one of the earliest changes in learning-dependent rewiring of the cortical column.Impact statementTactile learning is associated with reduced PV inhibition in superficial layers of somatosensory cortex. Modeling studies suggest that PV disinhibition can support prolonged recurrent activity initiated by thalamic input.

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Section: Introduction 40supporting

confidence: 59%

Section: Prolonged Sensory Association Training Reveals Multiple Stagmentioning

confidence: 97%

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Transient and layer-specific reduction in neocortical PV inhibition during sensory association learning

Kuljis

Park

Myal

et al. 2020

Preprint

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“…Primary and higher-order thalamocortical nuclei convey qualitatively different types of information 10,12,[18][19][20][21][22] , and we wondered if VP and POM communication with TRN might involve parallel differences in synaptic processing mechanisms. To address this, we compared the dynamic features of the glutamatergic synaptic currents (kinetics and short-term synaptic depression) evoked by photostimulating VP and POM inputs to central and edge TRN cells, respectively.…”

Section: Resultsmentioning

confidence: 99%

Two dynamically distinct circuits driving inhibition in sensory thalamus

Voelcker

Zaltsman

et al. 2020

Preprint

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Most sensory information destined for the neocortex is relayed there from the thalamus, where considerable transformation occurs 1,2 . One powerful means of transformation involves interactions between excitatory thalamocortical neurons that carry data to cortex and inhibitory neurons of the thalamic reticular nucleus (TRN) that regulate flow of those data 3-6 . Despite enduring recognition of the TRN's importance 7-9 , understanding of its cell types, their organization, and their functional properties has lagged that of the thalamocortical systems it controls.Here we address this, investigating somatosensory and visual circuits of the TRN. First, in the somatosensory TRN we observed two groups of genetically defined neurons that are topographically segregated, physiologically distinct, and connect reciprocally with independent thalamocortical nuclei via dynamically divergent synapses. Calbindin-expressing cells, located in the central core, connect with the ventral posterior nucleus (VP), the primary somatosensory thalamocortical relay. In contrast, somatostatin-expressing cells, residing along the surrounding edges of TRN, synapse with the posterior medial thalamic nucleus (POM), a higher-order structure that carries both top-down and bottom-up information 10-12 . The two TRN cell groups process their inputs in pathway-specific ways. Synapses from VP to central TRN cells evoke rapid currents that depress deeply during repetitive activity, driving phasic spike output. In contrast, synapses from POM to edge TRN cells evoke slower, sustained currents that drive more persistent spiking. Differences in intrinsic physiology of TRN cell types, including state-dependent bursting, also contribute to these output dynamics. Thus, processing specializations of the two TRN circuits appear to be tuned to the types of signals they carry-the primary central circuit to discrete sensory events, and the higher-order edge circuit to temporally distributed signals integrated from multiple sources. Central and edge circuits of the visual TRN and their associated thalamocortical nuclei closely resemble those of the somatosensory circuits. These results provide fundamental insights about how subnetworks of TRN neurons could differentially process distinct classes of thalamic information.

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“…A potential mechanism of this is that disinhibition of apical dendritic spikes leads to long-term potentiation of local recurrent synapses among cortical pyramidal neurons (Williams and Holtmaat, 2019). Furthermore, an in vivo study found that associative learning can also potentiate long-range POm connections onto pyramidal neurons when subsequently measured in vitro (Audette et al, 2019). Future studies are needed to address the links between arousal, attention, and plasticity.…”

Section: Discussionmentioning

confidence: 99%

Effects of arousal and movement on secondary somatosensory and visual thalamus

Petty

Kinnischtzke

Hong

et al. 2020

Preprint

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All neocortical sensory areas have an associated primary and secondary thalamic nucleus. While the primary nuclei encode sensory information and relay it to cortex, the drivers of activity in secondary nuclei are poorly understood. We recorded juxtasomally from neurons in secondary somatosensory (POm) and visual (LP) thalamic nuclei of awake head-fixed mice with simultaneous whisker tracking and pupilometry. POm activity correlated with the slow components of whisker movement but not fast precise kinematics. This movement modulation was not due to sensory reafference, persisting after unilateral paralysis of the whisker pad. POm tracked whisking even more strongly after optogenetic silencing of primary somatosensory and motor cortex, indicating that cortical motor efference copy cannot explain movement modulation. We observed that whisking and pupil dilation were strongly correlated, raising the possibility that POm tracks arousal rather than whisker movement. LP, being part of the visual system, is not expected to encode whisker movement. However, we discovered that LP and POm track whisking equally well, suggesting a global arousal effect on both nuclei. Our results suggest that motor signals are largely absent in POm. We conclude that global arousal may be a prominent modulator of secondary thalamic nuclei.

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Rapid Plasticity of Higher-Order Thalamocortical Inputs during Sensory Learning

Cited by 79 publications

References 61 publications

Transient and layer-specific reduction in neocortical PV inhibition during sensory association learning

Transient and layer-specific reduction in neocortical PV inhibition during sensory association learning

Two dynamically distinct circuits driving inhibition in sensory thalamus

Effects of arousal and movement on secondary somatosensory and visual thalamus

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