Neuronal mechanisms and attentional modulation of corticothalamic α oscillations

Abstract

Field potential oscillations in the ∼10 Hz range are known as the alpha rhythm. The genesis and function of alpha has been the subject of intense investigation for the past 80 years. Whereas early work focused on the thalamus as the pacemaker of alpha rhythm, subsequent slice studies revealed that pyramidal neurons in the deep layers of sensory cortices are capable of oscillating in the alpha frequency range independently. How thalamic and cortical generating mechanisms in the intact brain might interact to shape the organization and function of alpha oscillations remains unclear. We addressed this problem by analyzing laminar profiles of local field potential and multiunit activity (MUA) recorded with linear array multielectrodes from the striate cortex of two macaque monkeys performing an intermodal selective attention task. Current source density (CSD) analysis was combined with CSD-MUA coherence to identify intracortical alpha current generators and assess their potential for pacemaking. Coherence and Granger causality analysis was applied to delineate the patterns of interaction among different alpha current generators. We found that (1) separable alpha current generators are located in superficial, granular, and deep layers, with both layer 4C and deep layers containing primary local pacemaking generators, suggesting the involvement of the thalamocortical network, and (2) visual attention reduces the magnitude of alpha oscillations as well as the level of alpha interactions, consistent with numerous reports of occipital alpha reduction with visual attention in human EEG. There is also indication that alpha oscillations in the lateral geniculate cohere with those in V1.

Figure 1.

Time course of stimulus presentation in both the visual and auditory domain. The vertical bars represent stimuli, and deviant stimuli are indicated by arrows. The shaded interval before each standard visual stimulus defines the prestimulus time period of 200 ms in duration from which data were extracted for analysis in the attend-visual and ignore-visual conditions. For the auditory-only condition, no visual stimuli were presented.

Figure 2.

Alpha current generators from a typical penetration. A, Schematic of the multielectrode with 14 equally spaced (150 μm) contacts. B, A short segment (200 ms) of LFPs showing alpha oscillation. C, PRAT-CSD displayed as a color-coded plot, which is the second spatial derivative of phase-realigned and averaged PRAT-LFPs (smooth blue traces). The y-axis is electrode contacts from 2 to 13, with 2 being close to the cortical surface. A single epoch of MUA from three contacts is superimposed (black traces). D, Current source density profile of visual evoked activity. Laminar ERPs are overlaid (blue traces). The arrow marks the polarity inversion of the N40 component.

Figure 3.

Attentional modulation of alpha power. A, Average normalized LFP alpha peak power at the four alpha current generators located in layers 1/2, 3B/4A, 4C, and 6 under three experimental conditions. For each penetration, alpha peak power at each generator was divided by the alpha peak power at the layer 6 generator, and then averaged across eight penetrations. *p < 0.1; **p < 0.05; ***p < 0.01. B, Averaged CSD alpha peak power as a function of recording contacts and experimental conditions. CSD alpha power exhibited similar amplitude over penetrations, and thus no normalization was performed before averaging. Error bars indicate SEM.

Figure 4.

CSD–MUA coherence at the four alpha current generators identified by PRAT-CSD for the penetration shown in Figure 2.

Figure 5.

Pairwise CSD coherence spectra among the four alpha generators under three experimental conditions for the penetration shown in Figure 2.

Figure 6.

Granger causality analysis. A, Granger causality spectra for different alpha current generator pairs for the penetration in Figure 2. The y-axis is the driver and x-axis is the target (i.e., panel xy, where x is the row index of the panel and y is the column index, shows the Granger causality spectrum for y→x). B, Schematic representation of interaction between different alpha current generators. An arrow, understood in the sense of Granger causality, is plotted between two alpha current generators if more than one-half of the penetrations (n > 4) showed significant alpha Granger causality in that direction under the auditory-only condition.