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. 2013 Sep 11:4:603.
doi: 10.3389/fpsyg.2013.00603. eCollection 2013.

Desynchronization and rebound of beta oscillations during conscious and unconscious local neuronal processing in the macaque lateral prefrontal cortex

Theofanis I Panagiotaropoulos  1 , Vishal Kapoor, Nikos K Logothetis
Affiliations

Desynchronization and rebound of beta oscillations during conscious and unconscious local neuronal processing in the macaque lateral prefrontal cortex

Theofanis I Panagiotaropoulos et al. Front Psychol. .

Abstract

Accumulating evidence indicates that control mechanisms are not tightly bound to conscious perception since both conscious and unconscious information can trigger control processes, probably through the activation of higher-order association areas like the prefrontal cortex. Studying the modulation of control-related prefrontal signals in a microscopic, neuronal level during conscious and unconscious neuronal processing, and under control-free conditions could provide an elementary understanding of these interactions. Here we performed extracellular electrophysiological recordings in the macaque lateral prefrontal cortex (LPFC) during monocular physical alternation (PA) and binocular flash suppression (BFS) and studied the local scale relationship between beta (15-30 Hz) oscillations, a rhythmic signal believed to reflect the current sensory, motor, or cognitive state (status-quo), and conscious or unconscious neuronal processing. First, we show that beta oscillations are observed in the LPFC during resting state. Both PA and BFS had a strong impact on the power of this spontaneous rhythm with the modulation pattern of beta power being identical across these two conditions. Specifically, both perceptual dominance and suppression of local neuronal populations in BFS were accompanied by a transient beta desynchronization followed by beta activity rebound, a pattern also observed when perception occurred without any underlying visual competition in PA. These results indicate that under control-free conditions, at least one rhythmic signal known to reflect control processes in the LPFC (i.e., beta oscillations) is not obstructed by local neuronal, and accordingly perceptual, suppression, thus being independent from temporally co-existing conscious and unconscious local neuronal representations. Future studies could reveal the additive effects of motor or cognitive control demands on prefrontal beta oscillations during conscious and unconscious processing.

Keywords: beta oscillations; consciousness; control; prefrontal cortex.

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Figures

Figure 1
Figure 1
Behavioral task. In (A) monocular stimulation with a non-preferred pattern is followed by stimulation of the contralateral eye with a preferred visual stimulus. In (B) the order of visual stimulation is reversed. These PA conditions allowed us to study neurophysiological responses during purely sensory stimulation without any underlying competition. In (C) the non-preferred stimulus is suppressed by the presentation of a preferred visual pattern while in (D) the preferred pattern is suppressed due to a flash of the non-preferred. These BFS conditions that introduced visual competition allowed recordings during perceptual dominance and suppression of a local population. Therefore, BFS allowed us to study conscious and unconscious processing of a visual stimulus. Stimulus preference was determined by comparing the local population discharge response to the two stimuli used in (A) and (B) between t = 1301–2300 ms (see also Panagiotaropoulos et al., 2012).
Figure 2
Figure 2
(A) Power spectrum of resting-state activity in 45 recorded sites sorted according to the power magnitude at 22 Hz. All sites exhibit a prominent peak (black arrow) in the beta frequency range (approximately between 15 and 30 Hz). (B). Mean power spectrum ± s.e.m during resting state activity across the 45 recorded sites presented in (A). Note a bump (black arrow) in the mean power spectrum in the beta range. The peak in 50 Hz is due to power line noise.
Figure 3
Figure 3
Raw LFP traces (1–475 Hz) during PA (A,B) and BFS (C,D) for 10 trials from a typical prefrontal recording site. In (A), a non-preferred stimulus is presented in one eye and after 1 s is removed and a disparate pattern is presented in the contralateral eye. Using as a criterion the discharge response of the locally recorded population we determined that the second stimulus was the “preferred.” In (B) the order of visual stimulation is reversed and the preferred stimulus is followed by the presentation of the non-preferred. In (C,D) for BFS the order of stimulation is the same as in (A,B), respectively. However, in these trials the stimulus presented first is not removed but remains on and is suppressed by the stimulus presented between t = 1301–2300 ms (dominant stimulus-black, suppressed stimulus-gray). In both PA and BFS and for all conditions we can observe that the onset or change of visual stimulation results in a remarkable suppression of low frequency-high amplitude LFP components that rebound later when the stimulus remains on. These components are particularly dominant during the inter-trial period (t = 1301–2300).
Figure 4
Figure 4
Band-limited LFP signal (15–30 HZ) of the raw LFP signals presented in Figure 3. Beta oscillations are suppressed for all conditions during visual stimulation without any obvious relationship to stimulus preference for both PA (A and B) and BFS (C and D). Beta oscillations are particularly prominent during the inter-trial period.
Figure 5
Figure 5
Mean (across trials and recorded sites) time-frequency plot for PA and BFS. Following visual stimulation beta power exhibits desynchronization (white arrows in A) followed by a rebound of activity regardless of stimulus preference for both PA (A and B) and BFS (C and D). The frequency band is between 15 and 30 Hz.
Figure 6
Figure 6
Mean envelope (15–30 Hz) across trials and recorded sites for PA (A) and BFS (B). In PA there is no difference in the modulation of beta power between a switch from a preferred to a non-preferred (red curve) and a switch from a non-preferred to a preferred (blue curve) visual stimulus. Stimulus-induced desynchronization (black arrows) followed by a beta rebound is observed in both cases. The same pattern is observed during BFS (B). Note that in BFS from t = 1301–2300 there are no differences in beta power when the recorded neuronal population as well as the preferred pattern is dominant (blue) or suppressed (red).
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