Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques

Abstract

Field potential oscillations at approximately 10 Hz (alpha rhythm) are widely noted in the visual cortices, but their physiological mechanisms and significance are poorly understood. In vitro studies have implicated pyramidal neurons in both infragranular and supragranular layers as pacemakers. The generality of these observations for the intact brain in the behaving subject is unknown. We analyzed laminar profiles of spontaneous local field potentials and multiunit activity (MUA) recorded with linear array multielectrodes from visual areas V2, V4, and inferotemporal (IT) cortex of two macaque monkeys during performance of a sensory discrimination task. Current source density (CSD) analysis was combined with CSD-MUA coherence to identify intracortical alpha current generators and their potential for alpha pacemaking. The role of each alpha current generator was further delineated by Granger causality analyses. In V2 and V4, alpha current generators were found in all layers, with the infragranular generator acting as primary local pacemaking generator. In contrast, in IT, alpha current generators were found only in supragranular and infragranular layers, with the supragranular generator acting as primary local pacemaking generator. The amplitude of alpha activity in V2 and V4 was negatively correlated with behavioral performance, whereas the opposite was true in IT. The alpha rhythm in IT thus appears to differ from that in the lower-order cortices, both in terms of its underlying physiological mechanism and its behavioral correlates. This work may help to reconcile some of the diverse findings and conclusions on the functional significance of alpha band oscillations in the visual system.

Figure 1.

Results for V4. A, Schematic of the multielectrode with 14 equally spaced (200 μm) contacts. B, A short segment (200 ms) of LFPs. C, PRAT-CSD displayed as a color-coded plot, which is the second spatial derivative of phase-realigned and averaged PRAT-LFPs (smooth traces, blue). The y-axis is electrode contacts from 2 to 13. The contacts used for bipolar (bip) derivations are shown to the left (see Fig. 4 and Results, Interaction of alpha current generators). A single epoch of MUA from three contacts is superimposed (black). D, Laminar distribution of the peak (10 Hz) LFP power across all penetrations in both monkeys. E, CSD–MUA coherence spectra for the penetration shown in C. The horizontal line corresponds to p = 0.01.

Figure 2.

Results for V2. Gran, Granular. Conventions are otherwise the same as in Figure 1.

Figure 3.

Results for IT. cont., Contact; Gran, granular. Conventions are otherwise the same as in Figure 1.

Figure 4.

MVAR spectral analysis for the V4 penetration shown in Figure 1C. A, Power spectra of bipolar LFP signals at G and IG layers. B, Coherence spectrum between the two bipolar signals in A. C, D, Granger causality spectra between G and IG. Here, x→y denotes x driving y, and (x→y)/z denotes x driving y after conditioning out z. E, Power spectra of the bipolar LFP signals at SG and IG layers. F, Coherence spectrum between the two bipolar signals in E. G, H, Granger causality spectra between SG and IG. The horizontal lines in C, D, G, and H correspond to p = 0.01.

Figure 5.

MVAR spectral analysis for the V2 penetration shown in Figure 2A. Conventions are otherwise the same as in Figure 4.

Figure 6.

MVAR spectral analysis for the IT penetration shown in Figure 3A. Conventions are otherwise the same as in Figure 4.

Figure 7.

Schematic summarizing the results in V4 (left), V2 (middle), and IT (right). Layers containing alpha current generators are shaded in green. Arrows, depicting the interaction patterns among these generators, are understood in the sense of Granger causality. In V4 and V2, alpha current generators are found in SG, G, and IG layers, with the IG generator acting as the primary local alpha pacemaker. In IT, alpha current generators are found in SG and IG layers, with the SG generator acting as the primary local alpha pacemaker.

Figure 8.

Scatter plots showing strong correlation between alpha power and auditory reaction time in visual areas V4 (A), V2 (B), and IT (C). Insets, Spearman rank correlation coefficient. Linear least-squares best fits to the data are superimposed.