Thalamic bursting and the role of timing and synchrony in thalamocortical signaling in the awake mouse

Borden, Peter Y.; Nc, Wright; Morrissette, Arthur E.; Jaeger, Dieter; Haider, Bilal; Stanley, Garrett B.

doi:10.1016/j.neuron.2022.06.008

Cited by 30 publications

(30 citation statements)

References 103 publications

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“…The stimulus-evoked bursts in the thalamus and the resulting thalamo-cortical interaction, that primarily occur when the animal is in quiet wakefulness, result in longer, higher amplitude ERPs (Figure 7C and 7D). This is consistent with previous studies showing that stimulus-evoked bursting in thalamic relay neurons robustly activates cortical neurons (Borden et al, 2022; Nestvogel & McCormick, 2021; Ramcharan et al, 2005; Stoelzel et al, 2009; Swadlow & Gusev, 2001), with a cortical rebound depolarization lasting up to ∼0.5 s (Grenier et al, 1998), and 3-5 Hz cortical oscillation of ∼1 s median duration (Nestvogel & McCormick, 2021). Indeed, the more thalamic cells burst during the rebound period, the larger the magnitude of the second, late component in the ERP (Figure 6-figure supplement 2A).…”

Section: Discussionsupporting

confidence: 93%

“…Similarly, the CSD analysis generated results supporting our initial hypothesis. Thalamic bursts powerfully activate cortical neurons (Borden et al, 2022; Nestvogel & McCormick, 2021; Ramcharan et al, 2005; Sherman, 1996) via synaptic activity that can be captured by the inferred CSD. We observed a pronounced current sink near the border of layers 2/3 and 5 in MOs (near the deep stimulation site) that coincided with the timing of the thalamic rebound burst (~180 ms).…”

Section: Resultsmentioning

confidence: 99%

“…The thalamic spiking pattern evoked by deep stimulation during quiet wakefulness – brief excitation followed by a period of quiescence (74.6±15.5 ms) and a subsequent burst of action potentials – is consistent with previously described thalamic responses to cortical stimulation (Contreras & Steriade, 1995; Grenier et al, 1998). The fast action potential bursts in thalamic cells following the period of quiescence are likely to be triggered by low-threshold Ca 2+ spikes, known to follow periods of pronounced hyperpolarization in thalamic relay neurons (Borden et al, 2022; Contreras & Steriade, 1995; Grenier et al, 1998; Guido & Weyand, 1995; Halassa et al, 2011; Lu et al, 1992; Nestvogel & McCormick, 2021; Urbain et al, 2019). The thalamic silence-burst pattern may be a result of a withdrawal of excitation due to the cortical down-state or disynaptic inhibition via stimulation of thalamic reticular neurons, a primary source of GABAergic input to the thalamus (Bal et al, 2000; Domich et al, 1986; Pinault, 2004; Sherman & Guillery, 1996), both leading to the low-threshold Ca 2+ spike burst.…”

Section: Discussionmentioning

confidence: 99%

“…The fast action potential bursts in thalamic cells following the period of quiescence are likely to be triggered by low-threshold Ca 2+ spikes, known to follow periods of pronounced hyperpolarization in thalamic relay neurons (Borden et al, 2022;Contreras & Steriade, 1995;Grenier et al, 1998;Guido & Weyand, 1995;Halassa et al, 2011;Lu et al, 1992;Nestvogel & McCormick, 2021;Urbain et al, 2019).…”

Section: Electrically Evoked Spiking Pattern Depends On the Depth Of ...mentioning

confidence: 99%

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Cortico-thalamo-cortical interactions modulate electrically evoked EEG responses in mice

Claar

Rembado

Kuyat

et al. 2022

Preprint

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Perturbational complexity analysis predicts the presence of consciousness in humans by stimulating the brain with a brief pulse, recording cortical responses with electroencephalography (EEG), and measuring their spatiotemporal complexity. Measures reflecting perturbational complexity are low when consciousness vanishes in deep sleep, general anesthesia, or after widespread brain damage, and are high during wake, dreaming sleep and after recovery from brain injury. Here we examine the neural circuits underlying perturbational complexity in a mouse model by directly stimulating the cortex and recording high-density EEG, as well as spiking activity throughout the cortico-thalamo-cortical system with up to three Neuropixels probes, while subjects are awake or anesthetized via isoflurane. We find that when the mouse is awake, stimulation of deep cortical layers reliably evokes locally a brief pulse of excitation, followed by a bi-phasic sequence of a 120 ms profound off period and a rebound excitation. A similar pattern of spiking activity, some of which can be attributed to burst spiking, is seen in the connected thalamic nuclei. These spiking patterns are associated with a pronounced late component in the evoked EEG. We infer that cortico-thalamo-cortical interactions drive the long-lasting evoked EEG signals elicited by deep cortical stimulation during the awake state. The cortical and thalamic off period and rebound excitation, as well as the late component in the EEG, are reduced in running mice and are absent in animals anesthetized with isoflurane. This is also mirrored in the perturbational complexity indices computed during quiet wakefulness, running, and anesthetized states. Taken together, these results suggest that cortico-thalamo-cortical interactions contribute to ongoing activity in the conscious state that leads to highly complex global responses.

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Section: Discussionsupporting

confidence: 93%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Electrically Evoked Spiking Pattern Depends On the Depth Of ...mentioning

confidence: 99%

See 2 more Smart Citations

Cortico-thalamo-cortical interactions modulate electrically evoked EEG responses in mice

Claar

Rembado

Kuyat

et al. 2022

Preprint

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show abstract

“…Therefore, it is assumed that in the mammalian neocortex, information processing relies on the timing precision of neuronal activity within neuronal circuits and oscillators, [7][8][9][10][11][12][13][14][15][16][17] although firing rate is supposed to hold relevance. In this regard, the intrinsic timing of neuronal spiking seemingly depends on balanced subthreshold ionic currents (inward and outward) that shape the excitatory postsynaptic potentials (EPSP).…”

Section: Introductionmentioning

confidence: 99%

Timing to be precise? An overview of spike timing-dependent plasticity, brain rhythmicity, and glial cells interplay within neuronal circuits

2023

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In the mammalian brain information processing and storage rely on the complex coding and decoding events performed by neuronal networks. These actions are based on the computational ability of neurons and their functional engagement in neuronal assemblies where precise timing of action potential firing is crucial. Neuronal circuits manage a myriad of spatially and temporally overlapping inputs to compute specific outputs that are proposed to underly memory traces formation, sensory perception, and cognitive behaviors. Spike-timing-dependent plasticity (STDP) and electrical brain rhythms are suggested to underlie such functions while the physiological evidence of assembly structures and mechanisms driving both processes continues to be scarce. Here, we review foundational and current evidence on timing precision and cooperative neuronal electrical activity driving STDP and brain rhythms, their interactions, and the emerging role of glial cells in such processes. We also provide an overview of their cognitive correlates and discuss current limitations and controversies, future perspectives on experimental approaches, and their application in humans.

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Stimulus contrast modulates burst activity in the lateral geniculate nucleus

Sanchez

Alitto

Rathbun

et al. 2023

Current Research in Neurobiology

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Thalamic bursting and the role of timing and synchrony in thalamocortical signaling in the awake mouse

Cited by 30 publications

References 103 publications

Cortico-thalamo-cortical interactions modulate electrically evoked EEG responses in mice

Cortico-thalamo-cortical interactions modulate electrically evoked EEG responses in mice

Timing to be precise? An overview of spike timing-dependent plasticity, brain rhythmicity, and glial cells interplay within neuronal circuits

Stimulus contrast modulates burst activity in the lateral geniculate nucleus

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