Superior colliculus modulates cortical coding of somatosensory information

Gharaei, Saba; Honnuraiah, Suraj; Arabzadeh, Ehsan; Stuart, Gregory J

doi:10.1038/s41467-020-15443-1

Cited by 58 publications

(23 citation statements)

References 68 publications

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“…The above results are compatible with the view that top-down processes underlying beta event generated are recruited with temporal precision for attentional suppression of irrelevant information, perhaps mediated by the effects of superior colliculus on higher-order thalamic nuclei (Gharaei et al, 2020). In this case, the faciliatory Class 1 responses arising from stimulus/event coincidence could be interpreted as an "error" signal indicating that inhibition arrived too late, and that the beta event timing should be adjusted.…”

Section: Anticipatory Beta Events As a Predictive Signaling And Learning Mechanismsupporting

confidence: 82%

Thalamocortical mechanisms regulating the relationship between transient beta events and human tactile perception

Law

Pugliese

Shin

et al. 2021

Preprint

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Transient neocortical events with high spectral power in the 15-29Hz beta band are among the most reliable predictors of sensory perception. Prestimulus beta event rates in primary somatosensory cortex correlate with sensory suppression, most effectively 100-300ms before stimulus onset. However, the neural mechanisms underlying this perceptual association are unknown. We combined human magnetoencephalography (MEG) measurements with biophysical neural modeling to test potential cellular and circuit mechanisms that underlie observed correlations between prestimulus beta events and tactile detection. Extending prior studies, we found that simulated bursts from higher-order, non-lemniscal thalamus were sufficient to drive beta event generation and to recruit slow supragranular inhibition acting on a 300ms time scale to suppress sensory information. Further analysis showed that the same beta generating mechanism can lead to facilitated perception for a brief period when beta events occur simultaneously with tactile stimulation before inhibition is recruited. These findings were supported by close agreement between model-derived predictions and empirical MEG data. The post-event suppressive mechanism explains an array of studies that associate beta with decreased processing, while the during-event faciliatory mechanism may demand a reinterpretation of the role of beta events in the context of coincident timing.

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Section: Anticipatory Beta Events As a Predictive Signaling And Learning Mechanismsupporting

confidence: 82%

Thalamocortical mechanisms regulating the relationship between transient beta events and human tactile perception

Law

Pugliese

Shin

et al. 2021

Preprint

View full text Add to dashboard Cite

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“…However, the cuneate has also been observed to project to the posterior thalamic nucleus, although this observation applies to parts of the cuneate in which afferent with high precision information from digit 2 may possibly not exist ( Berkley et al, 1986 ). In terms of brainstem pathways, the cuneate output has a high number of potential indirect routes ( Loutit et al, 2021 ) to the thalamus, including the superior colliculus ( Bezdudnaya and Castro-Alamancos, 2011 ; Gharaei et al, 2020 ). The cerebellar nuclei can be provided with cutaneous input via spinal interneurons and the lateral reticular nucleus ( Bengtsson and Jorntell, 2014 ; Jorntell, 2017 ), and has powerful input to the motor thalamus (VL) ( Jorntell and Ekerot, 1999 ), which is a potential explanation for the decoding of tactile digit 2 information we observed in this part of the thalamus.…”

Section: Discussionmentioning

confidence: 99%

Widespread Decoding of Tactile Input Patterns Among Thalamic Neurons

Wahlbom

Enander

Jörntell

2021

Front. Syst. Neurosci.

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Whereas, there is data to support that cuneothalamic projections predominantly reach a topographically confined volume of the rat thalamus, the ventroposterior lateral (VPL) nucleus, recent findings show that cortical neurons that process tactile inputs are widely distributed across the neocortex. Since cortical neurons project back to the thalamus, the latter observation would suggest that thalamic neurons could contain information about tactile inputs, in principle regardless of where in the thalamus they are located. Here we use a previously introduced electrotactile interface for producing sets of highly reproducible tactile afferent spatiotemporal activation patterns from the tip of digit 2 and record neurons throughout widespread parts of the thalamus of the anesthetized rat. We find that a majority of thalamic neurons, regardless of location, respond to single pulse tactile inputs and generate spike responses to such tactile stimulation patterns that can be used to identify which of the inputs that was provided, at above-chance decoding performance levels. Thalamic neurons with short response latency times, compatible with a direct tactile afferent input via the cuneate nucleus, were typically among the best decoders. Thalamic neurons with longer response latency times as a rule were also found to be able to decode the digit 2 inputs, though typically at a lower decoding performance than the thalamic neurons with presumed direct cuneate inputs. These findings provide support for that tactile information arising from any specific skin area is widely available in the thalamocortical circuitry.

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“…In agreement with this finding, it is anatomically well described that S1, MI, and S2 receive thalamocortical projections from POm ( Ohno et al, 2012 ; El-Boustani et al, 2020 ), that they are, respectively, interhemispherically connected ( Carvell and Simons, 1987 ; Kinnischtzke et al, 2014 ) and that they have corticothalamic projections to POm ( Alloway et al, 2008 ; Liao et al, 2010 ). Moreover, POm is a strong driver of activity in S1, S2, and M1 ( Theyel et al, 2010 ; Gambino et al, 2014 ; Casas-Torremocha et al, 2019 ; Zhang and Bruno, 2019 ; Gharaei et al, 2020 ) and bilateral sensory responses in S2 have also been described ( Debowska et al, 2011 ).…”

Section: Discussionmentioning

confidence: 99%

Higher-Order Thalamic Encoding of Somatosensory Patterns and Bilateral Events

Castejon

Martín-Cortecero

Núñez

2021

Front. Neural Circuits

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The function of the higher-order sensory thalamus remains unclear. Here, the posterior medial (POm) nucleus of the thalamus was examined by in vivo extracellular recordings in anesthetized rats across a variety of contralateral, ipsilateral, and bilateral whisker sensory patterns. We found that POm was highly sensitive to multiwhisker stimuli involving diverse spatiotemporal interactions. Accurate increases in POm activity were produced during the overlapping time between spatial signals reflecting changes in the spatiotemporal structure of sensory patterns. In addition, our results showed for first time that POm was also able to respond to tactile stimulation of ipsilateral whiskers. This finding challenges the notion that the somatosensory thalamus only computes unilateral stimuli. We found that POm also integrates signals from both whisker pads and described how this integration is generated. Our results showed that ipsilateral activity reached one POm indirectly from the other POm and demonstrated a transmission of sensory activity between both nuclei through a functional POm-POm loop formed by thalamocortical, interhemispheric, and corticothalamic projections. The implication of different cortical areas was investigated revealing that S1 plays a central role in this POm-POm loop. Accordingly, the subcortical and cortical inputs allow POm but not the ventral posteromedial thalamic nucleus (VPM) to have sensory information from both sides of the body. This finding is in agreement with the higher-order nature of POm and can be considered to functionally differentiate and classify these thalamic nuclei. A possible functional role of these higher-order thalamic patterns of integrated activity in brain function is discussed.

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Superior colliculus modulates cortical coding of somatosensory information

Cited by 58 publications

References 68 publications

Thalamocortical mechanisms regulating the relationship between transient beta events and human tactile perception

Thalamocortical mechanisms regulating the relationship between transient beta events and human tactile perception

Widespread Decoding of Tactile Input Patterns Among Thalamic Neurons

Higher-Order Thalamic Encoding of Somatosensory Patterns and Bilateral Events

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