Crossmodal propagation of sensory-evoked and spontaneous activity in the rat neocortex

Abstract Peripheral neuropathies result in adaptation in primary sensory and other regions of cortex, and provide a framework for understanding the localized and widespread adaptations that arise from altered sensation. Mesoscale cortical imaging achieves high temporal resolution of activity using optical sensors of neuronal activity to simultaneously image across a wide expanse of cortex and capture this adaptation using sensory-evoked and spontaneous cortical activity. Saphenous nerve ligation in mouse is an animal model of peripheral neuropathy that produces hyperalgesia circumscribed to the hindlimb. We performed saphenous nerve ligation or sham, followed by mesoscale cortical imaging using voltage sensitive dye (VSD) after ten days. We utilized subcutaneous electrical stimulation at multiple stimulus intensities to characterize sensory responses after ligation or sham, and acquired spontaneous activity to characterize functional connectivity and large scale cortical network reorganization. Relative to sham animals, the primary sensory-evoked response to hindlimb stimulation in ligated animals was unaffected in magnitude at all stimulus intensities. However, we observed a diminished propagating wave of cortical activity at lower stimulus intensities in ligated animals after hindlimb, but not forelimb, sensory stimulation. We simultaneously observed a widespread decrease in cortical functional connectivity, where midline association regions appeared most affected. These results are consistent with localized and broad alterations in intracortical connections in response to a peripheral insult, with implications for novel circuit level understanding and intervention for peripheral neuropathies and other conditions affecting sensation.

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Spatiotemporal structure of sensory-evoked and spontaneous activity revealed by mesoscale imaging in anesthetized and awake mice

Cell Reports ◽

10.1016/j.celrep.2021.110081 ◽

2021 ◽

Vol 37 (10) ◽

pp. 110081

Author(s):

Navvab Afrashteh ◽

Samsoon Inayat ◽

Edgar Bermudez-Contreras ◽

Artur Luczak ◽

Bruce L. McNaughton ◽

...

Keyword(s):

Spontaneous Activity ◽

Spatiotemporal Structure ◽

Sensory Evoked

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Spatiotemporal structure of sensory-evoked and spontaneous activity revealed by mesoscale imaging in anesthetized and awake mice

10.1101/2020.05.22.111021 ◽

2020 ◽

Cited By ~ 1

Author(s):

Navvab Afrashteh ◽

Samsoon Inayat ◽

Edgar Bermudez Contreras ◽

Artur Luczak ◽

Bruce L. McNaughton ◽

...

Keyword(s):

Spontaneous Activity ◽

Brain Activity ◽

Activity Patterns ◽

Sensory Stimulation ◽

Wide Field ◽

Evoked Responses ◽

Evoked Activity ◽

Cortical Regions ◽

The One ◽

Sensory Evoked

AbstractBrain activity propagates across the cortex in diverse spatiotemporal patterns, both as a response to sensory stimulation and during spontaneous activity. Despite been extensively studied, the relationship between the characteristics of such patterns during spontaneous and evoked activity is not completely understood. To investigate this relationship, we compared visual, auditory, and tactile evoked activity patterns elicited with different stimulus strengths and spontaneous activity motifs in lightly anesthetized and awake mice using mesoscale wide-field voltage-sensitive dye and glutamate imaging respectively. The characteristics of cortical activity that we compared include amplitude, speed, direction, and complexity of propagation trajectories in spontaneous and evoked activity patterns. We found that the complexity of the propagation trajectories of spontaneous activity, quantified as their fractal dimension, is higher than the one from sensory evoked responses. Moreover, the speed and direction of propagation, are modulated by the amplitude during both, spontaneous and evoked activity. Finally, we found that spontaneous activity had similar amplitude and speed when compared to evoked activity elicited with low stimulus strengths. However, this similarity gradually decreased when the strength of stimuli eliciting evoked responses increased. Altogether, these findings are consistent with the fact that even primary sensory areas receive widespread inputs from other cortical regions, and that, during rest, the cortex tends to reactivate traces of complex, multi-sensory experiences that may have occurred in a range of different behavioural contexts.

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Spontaneous and sensory-evoked activity in mouse olfactory sensory neurons with defined odorant receptors

Journal of Neurophysiology ◽

10.1152/jn.00910.2012 ◽

2013 ◽

Vol 110 (1) ◽

pp. 55-62 ◽

Cited By ~ 30

Author(s):

Timothy Connelly ◽

Agnes Savigner ◽

Minghong Ma

Keyword(s):

Spontaneous Activity ◽

Odorant Receptor ◽

Odorant Receptors ◽

Spontaneous Firing ◽

Basal Activity ◽

Evoked Activity ◽

Sensory Evoked ◽

Noisy Background ◽

G Protein Coupled ◽

Spontaneous Firing Rate

Sensory systems need to tease out stimulation-evoked activity against a noisy background. In the olfactory system, the odor response profile of an olfactory sensory neuron (OSN) is dependent on the type of odorant receptor it expresses. OSNs also exhibit spontaneous activity, which plays a role in establishing proper synaptic connections and may also increase the sensitivity of the cells. However, where the spontaneous activity originates and whether it informs sensory-evoked activity remain unclear. We addressed these questions by examining patch-clamp recordings of genetically labeled mouse OSNs with defined odorant receptors in intact olfactory epithelia. We show that OSNs expressing different odorant receptors had significantly different rates of basal activity. Additionally, OSNs expressing an inactive mutant I7 receptor completely lacked spontaneous activity, despite being able to fire action potentials in response to current injection. This finding strongly suggests that the spontaneous firing of an OSN originates from the spontaneous activation of its G protein-coupled odorant receptor. Moreover, OSNs expressing the same receptor displayed considerable variation in their spontaneous activity, and the variation was broadened upon odor stimulation. Interestingly, there is no significant correlation between the spontaneous and sensory-evoked activity in these neurons. This study reveals that the odorant receptor type determines the spontaneous firing rate of OSNs, but the basal activity does not correlate with the activity induced by near-saturated odor stimulation. The implications of these findings on olfactory information processing are discussed.

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Network Mechanisms of Spindle-Burst Oscillations in the Neonatal Rat Barrel Cortex In Vivo

Journal of Neurophysiology ◽

10.1152/jn.00759.2006 ◽

2007 ◽

Vol 97 (1) ◽

pp. 692-700 ◽

Cited By ~ 112

Author(s):

Marat Minlebaev ◽

Yehezkel Ben-Ari ◽

Rustem Khazipov

Keyword(s):

Critical Period ◽

Developmental Plasticity ◽

Barrel Cortex ◽

Neonatal Rat ◽

Kainate Receptors ◽

Glutamatergic Synapses ◽

Rat Neocortex ◽

Gabaergic Synapses ◽

Sensory Evoked

Early in development, cortical networks generate particular patterns of activity that participate in cortical development. The dominant pattern of electrical activity in the neonatal rat neocortex in vivo is a spatially confined spindle-burst. Here, we studied network mechanisms of generation of spindle-bursts in the barrel cortex of neonatal rats using a superfused cortex preparation in vivo. Both spontaneous and sensory-evoked spindle-bursts were present in the superfused barrel cortex. Pharmacological analysis revealed that spindle-bursts are driven by glutamatergic synapses with a major contribution of AMPA/kainate receptors, but slight participation of NMDA receptors and gap junctions. Although GABAergic synapses contributed minimally to the pacing the rhythm of spindle-burst oscillations, surround GABAergic inhibition appeared to be crucial for their compartmentalization. We propose that local spindle-burst oscillations, driven by glutamatergic synapses and spatially confined by GABAergic synapses, contribute to the development of barrel cortex during the critical period of developmental plasticity.

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Spontaneous activity competes externally evoked responses in sensory cortex

10.1101/2020.08.18.256206 ◽

2020 ◽

Author(s):

Golan. Karvat ◽

Mansour Alyahyay ◽

Ilka Diester

Keyword(s):

Spontaneous Activity ◽

Brain Activity ◽

Detection Algorithm ◽

Dynamic State ◽

Evoked Responses ◽

Beta Band ◽

Beta Power ◽

Rat Somatosensory Cortex ◽

Sensory Evoked ◽

External Stimuli

SummaryThe functional role of spontaneous brain activity, especially in relation to external events, is a longstanding key question in neuroscience. Intrinsic and externally-evoked activities were suggested to be anticorrelated, yet inferring an antagonistic mechanism between them remains a challenge. Here, we used beta-band (15-30 Hz) power as a proxy of spontaneous activity in the rat somatosensory cortex during a detection task. Beta-power anticorrelated with sensory-evoked-responses, and high rates of spontaneously occurring beta-bursts predicted reduced detection. By applying a burst-rate detection algorithm in real-time and trial-by-trial stimulus-intensity adjustment, this influence could be counterbalanced. Mechanistically, bursts in all bands indicated transient synchronization of cell assemblies, but only beta-bursts were followed by a reduction in firing-rate. Our findings reveal that spontaneous beta-bursts reflect a dynamic state that competes with external stimuli.

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Visual experience sculpts whole-cortex spontaneous infraslow activity patterns through an Arc-dependent mechanism

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1711789114 ◽

2017 ◽

Vol 114 (46) ◽

pp. E9952-E9961 ◽

Cited By ~ 8

Author(s):

Andrew W. Kraft ◽

Anish Mitra ◽

Adam Q. Bauer ◽

Abraham Z. Snyder ◽

Marcus E. Raichle ◽

...

Keyword(s):

Spontaneous Activity ◽

Resting State ◽

Critical Period ◽

Visual Experience ◽

Visual Deprivation ◽

Critical Periods ◽

Sensory Evoked ◽

The Impact ◽

Dependent Mechanism ◽

Visual Network

Decades of work in experimental animals has established the importance of visual experience during critical periods for the development of normal sensory-evoked responses in the visual cortex. However, much less is known concerning the impact of early visual experience on the systems-level organization of spontaneous activity. Human resting-state fMRI has revealed that infraslow fluctuations in spontaneous activity are organized into stereotyped spatiotemporal patterns across the entire brain. Furthermore, the organization of spontaneous infraslow activity (ISA) is plastic in that it can be modulated by learning and experience, suggesting heightened sensitivity to change during critical periods. Here we used wide-field optical intrinsic signal imaging in mice to examine whole-cortex spontaneous ISA patterns. Using monocular or binocular visual deprivation, we examined the effects of critical period visual experience on the development of ISA correlation and latency patterns within and across cortical resting-state networks. Visual modification with monocular lid suturing reduced correlation between left and right cortices (homotopic correlation) within the visual network, but had little effect on internetwork correlation. In contrast, visual deprivation with binocular lid suturing resulted in increased visual homotopic correlation and increased anti-correlation between the visual network and several extravisual networks, suggesting cross-modal plasticity. These network-level changes were markedly attenuated in mice with genetic deletion of Arc, a gene known to be critical for activity-dependent synaptic plasticity. Taken together, our results suggest that critical period visual experience induces global changes in spontaneous ISA relationships, both within the visual network and across networks, through an Arc-dependent mechanism.

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