Delta-alpha/beta coupling as a signature of visual working memory in the prefrontal cortex

Abstract

Executive functions, particularly visual working memory, depend on the prefrontal cortex (PFC). Phase-amplitude coupling (PAC) has been proposed as a measure of synchronized brain oscillations. To study the neural correlates of working memory in cross-frequency interactions, local field potential (LFP) recordings were made in the PFC of two macaque monkeys. PAC analysis revealed that the delta band (1-5 Hz) phase modulated the alpha-beta band (8-33 Hz) amplitude throughout task epochs, in both the pre- and post-training stages. The elevation of δ-αβ PAC in the fixation period during post-training was a signature of task learning. Interestingly, the δ-αβ PAC was not enhanced in error trials compared to correct trials, and the subject's performance was strictly dependent on the orchestration of the delta phase. Furthermore, contrary to the dorsoventral functional specialization of PFC, spatial and shape stimuli induced the same pattern of PAC in PFC subdivisions.

Keywords: Biological sciences; Cell; Neuroscience.

Graphical abstract

Figure 1

Task and recording area Monkeys were trained to judge whether the cue and sample stimuli matched or did not match. (A) Spatial task: monkeys had to determine whether the location of the cue and sample stimuli, which had an identical shape, matched or not. (B) Shape task: the position of the stimuli remained constant in the shape task, where monkeys had to determine the matching status based on the shapes of the stimuli. Task steps indicated with yellow-colored boxes are not presented during the pre-training (passive) stage. (C) The anatomical location of the lateral prefrontal cortex sub-regions (for more details, see Figure S1).

Figure 2

PAC for spatial stimuli in the pre-training stage PAC maps were separately calculated for PFC subdivisions during the inter-trial (first column), the fixation (second column), the first delay (third column), and the second delay (fourth column) in the pre-training stage for the spatial set. (A) Posterior dorsal. (B) Medial dorsal. (C) Posterior ventral.

Figure 3

PAC for spatial stimuli in the post-training stage PAC maps were separately calculated for PFC subdivisions during the inter-trial (first column), the fixation (second column), the first delay (third column), and the second delay (fourth column) in the post-training stage for the spatial set. (A) Posterior dorsal. (B) Medial dorsal. (C) Posterior ventral.

Figure 4

δ-αβ PAC for spatial stimuli in PFC subdivisions Averaged δ-αβ PAC strength in PFC subdivisions is shown during the fixation, first delay, and second delay in pre- and post-training stages for spatial stimuli. The vertical black lines represent the standard error of the mean.

Figure 5

PAC of error trials during the post-training stage for spatial stimuli PAC maps of error trials were separately calculated for PFC subdivisions during the fixation (first column), the first delay (second column), and the second delay (third column) in the post-training stage for the spatial set. (A) Posterior dorsal. (B) Medial dorsal. (C) Posterior ventral.

Figure 6

PAC for shape stimuli in the post-training stage PAC maps were separately calculated for PFC subdivisions during the fixation (first column), the first delay (second column), and the second delay (third column) in the post-training stage for the shape set. (A) Posterior dorsal. (B) Medial dorsal. (C) Posterior ventral.

Figure 7

δ-αβ PAC scatterplot for spatial stimuli compared with shape stimuli Scatterplots of δ-αβ PAC for spatial and shape sets are shown separately for PFC subdivisions during the fixation (first column), the first delay (second column), and the second delay (third column) in the post-training stage for each recording channel. (A) Posterior dorsal. (B) Medial dorsal. (C) Posterior ventral. n = the number of channels, and p = the p-value (Wilcoxon signed-rank test).