Characterizing synchrony patterns across cognitive task stages of associative recognition memory

Abstract

Numerous studies seek to understand the role of oscillatory synchronization in cognition. This problem is particularly challenging in the context of complex cognitive behavior, which consists of a sequence of processing steps with uncertain duration. In this study, we analyzed oscillatory connectivity measures in time windows that previous computational models had associated with a specific sequence of processing steps in an associative memory recognition task (visual encoding, familiarity, memory retrieval, decision making, and motor response). The timing of these processing steps was estimated on a single‐trial basis with a novel hidden semi‐Markov model multivariate pattern analysis (HSMM‐MVPA) method. We show that different processing stages are associated with specific patterns of oscillatory connectivity. Visual encoding is characterized by a dense network connecting frontal, posterior, and temporal areas as well as frontal and occipital phase locking in the 4–9 Hz theta band. Familiarity is associated with frontal phase locking in the 9–14 Hz alpha band. Decision making is associated with frontal and temporo‐central interhemispheric connections in the alpha band. During decision making, a second network in the theta band that connects left‐temporal, central, and occipital areas bears similarity to the neural signature for preparing a motor response. A similar theta band network is also present during the motor response, with additionally alpha band connectivity between right‐temporal and posterior areas. This demonstrates that the processing stages discovered with the HSMM‐MVPA method are indeed linked to distinct synchronization patterns, leading to a closer understanding of the functional role of oscillations in cognition.

Orchestration of brain oscillations: principles and functions

“…() suggests that alpha desynchronization reflects continuous engagement of the visual system during auditory‐visual multisensory integration. However, in the current special issue and elsewhere, multiple empirical studies suggest a more nuanced view on the role of alpha modulation in cognitive processes such as in memory encoding (Portoles et al ., ), memory retention (Portoles et al ., ; Schroeder et al ., ), speech segmentation (Shahin & Pitt, ), task‐set switching (Foxe et al ., ; Portoles et al ., ), and selective auditory attention (Tune et al ., ). Another such example comes from the lesion study reported herein by Piai et al .…”

Data-Driven Classification of Spectral Profiles Reveals Brain Region-Specific Plasticity

“…Various studies have observed that brain rhythms are recruited in a task-specific manner during sensory, motor and higher-cognitive tasks, linking intrinsic brain rhythms to cognitive functions (Engel et al 1992; Singer and Gray 1995; Engel et al 2001; Lakatos et al 2008; Holcombe 2009; Giraud and Poeppel 2012; Lakatos et al 2013; Heusser et al 2016; Portoles et al 2018; Rimmele, Gross, et al 2018; Schroeder et al 2018; VanRullen 2018). For instance, in sighted individuals, the role of the alpha rhythm (~8–12Hz) in cognition is well-established, with posterior alphaand gamma-band oscillations coupling in excitatory-inhibitory cycles (Klimesch et al 2007; Buffalo et al 2011; Jensen et al 2012).…”

Modulations of local synchrony over time lead to resting-state functional connectivity in a parsimonious large-scale brain model

“…One may argue that a limitation or virtue of this LSBM is that it models only one frequency band but not the whole power spectrum of MEG. Yet, MEG is typically analyzed in frequency bands which each seem to play distinct functional roles [3,5,7,25,[62][63][64]. During behavioral tasks as well as resting-state each frequency band tends to produce a different FC pattern [3,7,64].…”

“…Yet, MEG is typically analyzed in frequency bands which each seem to play distinct functional roles [3,5,7,25,[62][63][64]. During behavioral tasks as well as resting-state each frequency band tends to produce a different FC pattern [3,7,64]. Moreover, behavioral studies analyze event related synchronization within one frequency band [5,25,65].…”

“…A fundamental limitation is that the macroscopic variables cannot describe within-ensemble modulations of synchronization [5,12,24]. Yet, it is exactly these fluctuations of local synchrony (often referred to as event-related synchronization/desynchronization) that characterize behavioral tasks [25], and are associated with changes in functional connectivity between brain regions during tasks and on-going activity [3,4].…”