Thalamocortical Mechanisms Regulating the Relationship between Transient Beta Events and Human Tactile Perception

Abstract

Transient neocortical events with high spectral power in the 15–29 Hz 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 100–300 ms 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, nonlemniscal thalamus were sufficient to drive beta event generation and to recruit slow supragranular inhibition acting on a 300 ms timescale 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 postevent suppressive mechanism explains an array of studies that associate beta with decreased processing, whereas the during-event facilitatory mechanism may demand a reinterpretation of the role of beta events in the context of coincident timing.

Cortical response variability is driven by local excitability changes with somatotopic organization

“…In another approach, attempting to account for possible differences of hand and foot oscillatory networks, we extended our analyses of pre-stimulus alpha activity (8 to 13 Hz) to the beta frequency band (18 to 23 Hz), the second major frequency component of the somatosensory mu rhythm, which has been associated with a similar (yet not identical) modulatory role as alpha activity in somatosensory perception (Anderson and Ding, 2011; Jones et al, 2010; Law et al, 2021; van Ede et al, 2010). Here, we indeed found somatotopic effects of pre-stimulus amplitude on P40 amplitude also in the tibial-only condition over more medial regions, presumably corresponding to foot regions, thus contrasting the spatial effect patterns over hand regions in the alpha frequency band.…”

Spatiotemporal organization of human sensorimotor beta burst activity

“…This view sides with the proposed akinetic role of high sensorimotor beta states (Gilbertson et al, 2005;Joundi et al, 2012;Khanna & Carmena, 2017;Pogosyan et al, 2009). However, burst activity may have heterogenous and mechanistically distinct components which can be characterised by their distinct spatial, temporal, and spectral structure (Law et al, 2022;Zich et al, 2020) that, in addition to zero-lagged activity, contains spatiotemporal gradients, or travelling wave, components. In animals, for example, a high proportion of sensorimotor beta activity occurs as travelling waves (Rubino et al, 2006;Rule et al, 2018), in addition to highly synchronous standing waves.…”

“…Sensorimotor beta burst activity is commonly considered as zero-lagged (or standing wave) activity which is generated by the summation of synchronized layer-specific inputs within cortical columns that result in a cumulative dipole with a stereotypical wavelet shape in the time domain (Bonaiuto et al, 2021; Law et al, 2022; Neymotin et al, 2020). These time-periods of synchronous activity which generate standing wave activity are thought to convey little information encoding (Brittain & Brown, 2014; Carhart-Harris, 2018; Carhart-Harris et al, 2014).…”

Resolving the mesoscopic missing link: Biophysical modeling of EEG from cortical columns in primates

“…Recent studies have linked transmembrane currents of pyramidal cells (PC) to equivalent dipoles and the dipoles to macroscopic EEG signals (Jones et al, 2009(Jones et al, , 2007Kohl et al, 2022;Law et al, 2022;Naess et al, 2021). Information derived from local field potentials (LFP) sampled across all the layers of the cerebral cortex can validate these equivalent dipoles (Murakami and Okada, 2006;Riera et al, 2012).…”

“…Detailed biophysical models of populations of neurons offer insights into the relationship between microscopic transmembrane currents and macroscopic cranial voltages through forward modeling (Cohen, 2017; Einevoll et al, 2019; Næss et al, 2021; Pesaran et al, 2018). Recent studies have linked transmembrane currents of pyramidal cells (PC) to equivalent dipoles and the dipoles to macroscopic EEG signals (Jones et al, 2009, 2007; Kohl et al, 2022; Law et al, 2022; Næss et al, 2021). Information derived from local field potentials (LFP) sampled across all the layers of the cerebral cortex can validate these equivalent dipoles (Murakami and Okada, 2006; Riera et al, 2012).…”