Layer-Specific Entrainment of Gamma-Band Neural Activity by the Alpha Rhythm in Monkey Visual Cortex

Abstract

Summary While the mammalian neocortex has a clear laminar organization, layer-specific neuronal computations remain to be uncovered. Several studies suggest that gamma band activity in primary visual cortex (V1) is produced in granular and superficial layers and is associated with the processing of visual input [1–3]. Oscillatory alpha band activity in deeper layers has been proposed to modulate neuronal excitability associated with changes in arousal and cognitive factors [4–7]. To investigate the layer-specific interplay between these two phenomena, we characterized the coupling between alpha and gamma band activity of the local field potential (LFP) in V1 of the awake macaque. Using multicontact laminar electrodes to measure spontaneous signals simultaneously from all layers of V1, we found a robust coupling between alpha phase in the deeper layers and gamma amplitude in granular and superficial layers. Moreover, the power in the two frequency bands was anticorrelated. Taken together, these findings demonstrate robust inter-laminar cross-frequency coupling in the visual cortex, supporting the view that neuronal activity in the alpha frequency range phasically modulates processing in the cortical microcircuit in a top-down manner [7].

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

“…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.…”

“…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).…”

Sensory-driven and spontaneous gamma oscillations engage distinct cortical circuitry

“…Similarly, in vivo experiments demonstrate coherence in the gamma band either among superficial-layer LFPs or among deep-layer LFPs, with a distinct transition between the two zones in the thalamorecipient layers (Maier et al 2010). Supra-and infragranular-layer gamma oscillations were differentially modulated by ongoing alpha oscillations in the awake, behaving macaque, providing evidence for laminar specificity in gamma activity (Spaak et al 2012). Additionally, in both in vitro studies, superficial-layer gamma was dependent on chloride GABAergic transmission.…”

Long-range intralaminar noise correlations in the barrel cortex

“…It has been well established that the layers vary in the relative proportions of their cell types (Ciceri et al 2013) and in the expression of receptors and other proteins (Nelson et al 2006;Watakabe et al 2006;Yamamori and Rockland 2006). Functionally, it has been noted that different layers within the same region are able to produce specific aspects of the networks' oscillatory activity (Silva et al 1991;Buffalo et al 2011;Spaak et al 2012;Beltramo et al 2013). Thus it is not surprising that different layers contribute differently to sensory responses (Hirsch and Martinez 2006;Self et al 2013).…”