Laminar Profile and Physiology of the α Rhythm in Primary Visual, Auditory, and Somatosensory Regions of Neocortex

Abstract

The functional significance of the ␣ rhythm is widely debated. It has been proposed that ␣ reflects sensory inhibition and/or a temporal sampling or "parsing" mechanism. There is also continuing disagreement over the more fundamental questions of which cortical layers generate ␣ rhythms and whether the generation of ␣ is equivalent across sensory systems. To address these latter questions, we analyzed laminar profiles of local field potentials (LFPs) and concomitant multiunit activity (MUA) from macaque V1, S1, and A1 during both spontaneous activity and sensory stimulation. Current source density (CSD) analysis of laminar LFP profiles revealed ␣ current generators in the supragranular, granular, and infragranular layers. MUA phase-locked to local current source/sink configurations confirmed that ␣ rhythms index local neuronal excitability fluctuations. CSD-defined ␣ generators were strongest in the supragranular layers, whereas LFP ␣ power was greatest in the infragranular layers, consistent with some of the previous reports. The discrepancy between LFP and CSD findings appears to be attributable to contamination of the infragranular LFP signal by activity that is volume-conducted from the stronger supragranular ␣ generators. The presence of ␣ generators across cortical depth in V1, S1, and A1 suggests the involvement of ␣ in feedforward as well as feedback processes and is consistent with the view that ␣ rhythms, perhaps in addition to a role in sensory inhibition, may parse sensory input streams in a way that facilitates communication across cortical areas.

The relationship between oscillatory EEG activity and the laminar-specific BOLD signal

“…Our finding that α-oscillations are related to activity in deep layers agrees well with various laminar studies reporting α-activity in infragranular layers (6,7,9,12). However, we did not find a relation between the attention effects in BOLD and α-power in the deep layers.…”

“…This difference suggests multiple neural processes related to α-activity within the visual cortex as measured at the scalp with EEG. Although some studies have demonstrated multiple α-sources in the early visual regions in both supra-and infragranular layers (9,12), others suggested a predominance of α-activity in deep layers (6,11,31). The results here are in line with multiple α-sources in both supraand infragranular layers, in which, in our task, only the α-source or sources in more superficial layers are modulated by attention.…”

“…This finding is supported by laminar recordings in animals reporting both supraand infragranular sources (9,12) and relating α-activity to feedback projections that target both supra-and infragranular layers (4). Consistently, laminar fMRI work has linked feedback processes to both superficial (17) and deep layers (18).…”

“…Intracranial electrophysiological recordings in animals have linked neuronal oscillations in different frequency bands to the cortical feedforward and feedback information flow and to cortico-subcortical interactions (2)(3)(4)(5). In line with these findings, electrophysiological recordings in animals have also demonstrated that changes in α-, β-, and γ-bands can be localized to specific cortical layers (6)(7)(8)(9)(10)(11)(12).…”

MEG-measured visually induced gamma-band oscillations in chronic schizophrenia: Evidence for impaired generation of rhythmic activity in ventral stream regions

“…Alpha generators have been found in different layers of both striate and extra-striate visual areas (Bollimunta et al, 2008(Bollimunta et al, , 2011Mo et al, 2011;Haegens et al, 2015;van Kerkoerle et al, 2014), and are known to be modulated in activity by both cortico-cortical and recurrent thalamo-cortical (TC) communication (Steriade et al, 1990), influenced by thalamic nuclei such as the lateral geniculate nucleus (LGN), the pulvinar nucleus, and the thalamic reticular nucleus (TRN). Evidence is growing that these different thalamic nuclei play different roles in sensory information processing, both spatially (i.e., across the visual hierarchy) and temporally (i.e., during early feedforward and later feedback processing), raising the possibility that aberrant alpha-band activity in visual cortices may in part reflect aberrant TC-interactions.…”