Traveling waves in the prefrontal cortex during working memory

Bhattacharya, Sayak; Brincat, Scott L.; Lundqvist, Mikael; Miller, Earl K.

doi:10.1371/journal.pcbi.1009827

Cited by 67 publications

(68 citation statements)

References 45 publications

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“…This interpretation is also consistent with earlier work showing that different patterns of neuronal oscillations modulate feedforward networks during visual perception 51,54 and as well as feedback processing during top-down control and prediction 55 . Consistent with our results, there is also other evidence of neural activity changing direction for specific functional states 25,44,[56][57][58][59][60] , thus suggesting that our results are part of a broader phenomenon.…”

Section: Discussionsupporting

confidence: 92%

The direction and timing of theta and alpha traveling waves modulate human memory processing

Mohan

Zhang

Jacobs

2022

Preprint

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To support a range of behaviors, the brain must flexibly coordinate neural activity across widespread brain regions. One potential mechanism for this coordination is a traveling wave, in which a neural oscillation propagates across the brain while organizing the order and timing of activity across regions (Ermentrout & Kleinfeld, 2001; Muller et al., 2018). Although traveling waves are present across the brain in various species (Lubenov & Siapas, 2009; Zhang et al., 2018; Davis et al., 2020), their potential functional relevance remained unknown. Here, using rare direct human brain recordings, we demonstrate two novel functional roles for traveling waves of theta- and alpha-band (2-13 Hz) oscillations in the cortex. First, traveling waves propagate in different directions during separate cognitive processes. In episodic memory, traveling waves tended to propagate in posterior-to-anterior and anterior-to-posterior directions, respectively, during encoding and retrieval. Second, traveling waves are informative about the timing of behavior, with the phase of ongoing traveling waves indicating when subjects would retrieve memories. Because traveling waves of oscillations correspond to local neuronal spiking, these patterns indicate that rhythmic pulses of activity move across the brain with different directions and timing for separate behaviors. More broadly, our results suggest a fundamental role for traveling waves and oscillations in dynamically coordinating neural connectivity, by flexibly organizing the timing and directionality of network interactions across the cortex to support cognition and behavior.

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Section: Discussionsupporting

confidence: 92%

The direction and timing of theta and alpha traveling waves modulate human memory processing

Mohan

Zhang

Jacobs

2022

Preprint

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“…Our finding that TWs were strongest in the beta frequency band (10–30 Hz) is consistent with a long line of work linking frontal beta-band oscillations with cognitive control and working memory (Babapoor-Farrokhran et al, 2017; Bhattacharya et al, 2022; Brincat and Miller, 2015; Miller et al, 2018; Womelsdorf, 2021). Studies have also suggested that beta-band oscillations behave as propagating TWs in sensory, motor and premotor structures (e.g., in humans ((Stolk et al, 2019; Takahashi et al, 2011), monkeys (Rubino et al, 2006; Takahashi et al, 2015), and cats (Roelfsema et al, 1997))).…”

Section: Discussionsupporting

confidence: 91%

“…On the other hand, rather than being uniformly distributed, TWs propagated primarily along two directions aligned with one spatial axis. This pattern may indicate preferential connectivity along anatomical axes orthogonal to a sulcus (Rubino et al, 2006) or, alternatively, may be due to the fact that our microarrays provided a narrow view, through a ∼10 mm 2 aperture, into what may have been a more complex (e.g., spiral or circular) pattern over larger cortical areas (Bhattacharya et al, 2022; Ermentrout and Kleinfeld, 2001).…”

Section: Discussionmentioning

confidence: 99%

Traveling waves in the monkey frontoparietal network predict recent reward memory

Zabeh

Foley

Jacobs

et al. 2022

Preprint

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Brain function depends on neural communication, but the mechanisms of this communication are not well understood. Recent studies suggest that one form of neural communication is through traveling waves (TWs)-patterns of neural oscillations that propagate within and between areas. We show that TWs appear robustly in microarray recordings in monkey frontal and parietal cortex and encode memory for recent rewards. While making saccades to obtain probabilistic rewards, monkeys were sensitive to the (statistically irrelevant) prior reward, which is consistent with behavioral biases produced by reward history. TWs in frontal and parietal areas were stronger in trials following a prior reward versus a lack of reward and, in the frontal lobe, correlated with the monkeys' sensitivity to the prior reward. The findings suggest that neural communication across fronto-parietal areas, reflected by TWs, maintains default reward memories, while communication within the frontal lobe mediates the read out of the memories for prospective expectations.

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“…Propagating wave activity can occur in a wide range of different speeds, with propagation speeds broadly falling into two categories. Speeds for mesoscopic traveling waves occurring within cortical columns and their lateral connections, as identified using local field potential (LFP), multielectrode arrays or optical imaging, and range between 0.1-0.8m/s (Bhattacharya et al, 2022; Rubino et al, 2006; Takahashi et al, 2011, 2015). These slower wave speeds are consistent with axonal conduction speeds of unmyelinated horizontal fibres in the superficial layers of the cortex (Girard et al, 2001).…”

Section: Discussionmentioning

confidence: 99%

Spatiotemporal organization of human sensorimotor beta burst activity

Zich

Quinn

Bonaiuto

et al. 2022

Preprint

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Beta oscillations in human sensorimotor cortex are hallmark signatures of healthy and pathological movement. In single trials, beta oscillations include bursts of intermittent, transient periods of high-power activity. These burst events have been linked to a range of sensory and motor processes, but their precise spatial, spectral, and temporal structure remains unclear. Specifically, a role for beta burst activity in information coding and communication suggests spatiotemporal patterns, or travelling wave activity, along specific anatomical gradients. We here show in human magnetoencephalography recordings that burst activity in sensorimotor cortex occurs in planar spatiotemporal wave-like patterns that dominate along two axes either parallel or perpendicular to the central sulcus. Moreover, we find that the two propagation directions are characterised by distinct anatomical and physiological features. Finally, our results suggest that sensorimotor beta bursts occurring before and after a movement share the same generator but can be distinguished by their anatomical, spectral and spatiotemporal characteristics, indicating distinct functional roles.

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Traveling waves in the prefrontal cortex during working memory

Cited by 67 publications

References 45 publications

The direction and timing of theta and alpha traveling waves modulate human memory processing

The direction and timing of theta and alpha traveling waves modulate human memory processing

Traveling waves in the monkey frontoparietal network predict recent reward memory

Spatiotemporal organization of human sensorimotor beta burst activity

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