Burst Firing Synchronizes Prefrontal and Anterior Cingulate Cortex during Attentional Control

Womelsdorf, Thilo; Ardid, Salva; Everling, Stefan; Valiante, Taufik A.

doi:10.1016/j.cub.2014.09.046

Cited by 107 publications

(123 citation statements)

References 44 publications

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“…Beta expression and its coherence between distinct brain foci are thought to contribute to information processing at several levels, including communication between neocortical areas (3,8,12), the protection of current behavioral and processing states from interruption (11), and memory maintenance. Our results provide a unifying link between studies suggesting that beta coordination mediates top-down neocortical processing (11,12,60) and studies showing that top-down influences are communicated through supragranular layers (61), because the described beta mechanism is explicitly dependent on strong excitatory synaptic drive to supragranular layers. A key unifying theme for sensorimotor beta expression is its negative correlation with active processing (7,11,18).…”

Section: Discussionsupporting

confidence: 64%

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice

Sherman

Lee

Law

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

415

510

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Human neocortical 15-29-Hz beta oscillations are strong predictors of perceptual and motor performance. However, the mechanistic origin of beta in vivo is unknown, hindering understanding of its functional role. Combining human magnetoencephalography (MEG), computational modeling, and laminar recordings in animals, we present a new theory that accounts for the origin of spontaneous neocortical beta. In our MEG data, spontaneous beta activity from somatosensory and frontal cortex emerged as noncontinuous beta events typically lasting <150 ms with a stereotypical waveform. Computational modeling uniquely designed to infer the electrical currents underlying these signals showed that beta events could emerge from the integration of nearly synchronous bursts of excitatory synaptic drive targeting proximal and distal dendrites of pyramidal neurons, where the defining feature of a beta event was a strong distal drive that lasted one beta period (∼50 ms). This beta mechanism rigorously accounted for the beta event profiles; several other mechanisms did not. The spatial location of synaptic drive in the model to supragranular and infragranular layers was critical to the emergence of beta events and led to the prediction that beta events should be associated with a specific laminar current profile. Laminar recordings in somatosensory neocortex from anesthetized mice and awake monkeys supported these predictions, suggesting this beta mechanism is conserved across species and recording modalities. These findings make several predictions about optimal states for perceptual and motor performance and guide causal interventions to modulate beta for optimal function. beta rhythm | magnetoencephalography | computational modeling | sensorimotor processing | Parkinson's disease B eta band rhythms (15-29 Hz) are a commonly observed activity pattern in the brain. They are found with magnetoencephalography (MEG) (1-4), EEG (5, 6), and local field potential (LFP) recordings from neocortex (7-9) and are preserved across species (10). Local beta oscillations and their coordination between regions are implicated in numerous functions, including sensory perception, selective attention, and motor planning and initiation (2,3,6,7,9,(11)(12)(13)(14)(15). Neocortical beta oscillations are disrupted in various neuropathologies, most notably Parkinson's disease (PD), in which treatments that alleviate motor symptoms also reverse the neocortical beta disruption (16,17). Although associations between beta and performance suggest a crucial role in brain function, beta rhythmicity might not be important per se but instead may be an epiphenomenal consequence of other important processes. Discovering how beta emerges at the cellular and network levels is crucial to understanding why beta is such a clear predictor of performance in many domains.A major, unresolved point of debate concerns the locus of beta generation. One prominent view is that beta is generated in basal ganglia and thalamic structures and that neocortical beta is an entrained reflecti...

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Section: Discussionsupporting

confidence: 64%

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice

Sherman

Lee

Law

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

415

510

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“…For instance, increased theta band phase coherence between ACC and lateral PFC (lPFC) electrodes was found previously in humans and macaques performing different tasks that probed cognitive control and task-switching abilities (Cavanagh et al, 2009;Phillips et al, 2014). Previous findings in the macaque suggest that the interaction between lateral PFC areas and ACC can be traced back to the burst firing events of cells in ACC, with bursts in the ACC synchronizing to the LFP in PFC during attentional states (Womelsdorf et al, 2014a). These findings provide compelling evidence for the existence of direct communication between the ACC and PFC during attentional control.…”

Section: Introductionmentioning

confidence: 79%

“…One possible mechanism is that neurons across these brain areas synchronize their firing to delegate information. The communication between the PFC subareas and the ACC has been tested by a few studies that used electroencephalography (Cavanagh et al, 2009) or local field potential (LFP) measures (Tsujimoto et al, 2006;Rothé et al, 2011;Womelsdorf et al, 2014a). For instance, increased theta band phase coherence between ACC and lateral PFC (lPFC) electrodes was found previously in humans and macaques performing different tasks that probed cognitive control and task-switching abilities (Cavanagh et al, 2009;Phillips et al, 2014).…”

Section: Introductionmentioning

confidence: 98%

Interareal Spike-Train Correlations of Anterior Cingulate and Dorsal Prefrontal Cortex during Attention Shifts

et al. 2015

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The anterior cingulate cortex (ACC) and prefrontal cortex (PFC) are believed to coactivate during goal-directed behavior to identify, select, and monitor relevant sensory information. Here, we tested whether coactivation of neurons across macaque ACC and PFC would be evident at the level of pairwise neuronal correlations during stimulus selection in a spatial attention task. We found that firing correlations emerged shortly after an attention cue, were evident for 50 -200 ms time windows, were strongest for neuron pairs in area 24 (ACC) and areas 8 and 9 (dorsal PFC), and were independent of overall firing rate modulations. For a subset of cell pairs from ACC and dorsal PFC, the observed functional spike-train connectivity carried information about the direction of the attention shift. Reliable firing correlations were evident across area boundaries for neurons with broad spike waveforms (putative excitatory neurons) as well as for pairs of putative excitatory neurons and neurons with narrow spike waveforms (putative interneurons). These findings reveal that stimulus selection is accompanied by slow time scale firing correlations across those ACC/PFC subfields implicated to control and monitor attention. This functional coupling was informative about which stimulus was selected and thus indexed possibly the exchange of task-relevant information. We speculate that interareal, transient firing correlations reflect the transient coordination of larger, reciprocally interacting brain networks at a characteristic 50 -200 ms time scale.

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“…In the following, we report results pooled across monkeys and show that individual monkey results were consistent and qualitatively similar in SI Result S1. These recordings were from a dataset that was previously analyzed with respect to neuronal firing and burst-LFP synchronization (3,12,13) (SI Methods). During each trial, covert spatial attention had to be shifted toward one of two peripheral stimuli in response to the color of a centrally presented cue stimulus (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Although overall firing-rate modulations of neurons were not statistically associated with theta-gamma correlations (SI Result S12), it is possible that finer-grained burst firing events relate to long-range theta-gamma correlations, similar to burst firing events synchronizing long-range to midgamma-band (55-75 Hz) LFP activity (12). We thus correlated burst-LFP synchronization of neurons recorded at LFP recording sites that provided theta-phase or gamma-amplitude variations for theta-gamma correlations (SI Result S13).…”

Section: Theta-gamma Correlation and Its Relation To Synchronization Ofmentioning

confidence: 99%

Theta–gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts

Voloh

Valiante

Everling

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Anterior cingulate and lateral prefrontal cortex (ACC/PFC) are believed to coordinate activity to flexibly prioritize the processing of goal-relevant over irrelevant information. This between-area coordination may be realized by common low-frequency excitability changes synchronizing segregated high-frequency activations. We tested this coordination hypothesis by recording in macaque ACC/PFC during the covert utilization of attention cues. We found robust increases of 5-10 Hz (theta) to 35-55 Hz (gamma) phaseamplitude correlation between ACC and PFC during successful attention shifts but not before errors. Cortical sites providing theta phases (i) showed a prominent cue-induced phase reset, (ii) were more likely in ACC than PFC, and (iii) hosted neurons with burst firing events that synchronized to distant gamma activity. These findings suggest that interareal theta-gamma correlations could follow mechanistically from a cue-triggered reactivation of rule memory that synchronizes theta across ACC/PFC.T he anterior cingulate and prefrontal cortex (ACC/PFC) of primates are key structures that ensure the flexible deployment of attention during goal-directed behavior (1, 2). To achieve such flexible control, diverse streams of information need to be taken into account, which are encoded by neuronal populations in anatomically segregated subfields of the ACC/ PFC (3, 4). Information about the expected values of possible attentional targets are prominently encoded in medial prefrontal cortices and ACC, whereas the rules and task goals that structure goal-directed behavior are prominently encoded in the lateral PFC (5, 6). Flexible biasing of attention thus requires the integration of information across anatomically segregated cortical circuits. One candidate means to achieve such interareal integration is by synchronizing local processes in distant brain areas to a common process. A rich set of predominantly rodent studies have documented such interareal neuronal interactions in the form of a phase-amplitude (P-A) correlations between lowfrequency periodic excitability fluctuation and high-frequency gamma-band activity (7-9). It is, however, unknown whether there are reliable cross-frequency P-A interactions between those primate ACC/PFC nodes that underlie flexible attention shifts and, if so, whether P-A correlations are reliably linked to the actual successful deployment of attention (10, 11). We thus set out to test for and characterize P-A interactions during covert control processes by recording local field potential (LFP) activity in macaque ACC/PFC subfields during attentional stimulus selection. ResultsWe recorded LFP activity from 1,104 between-channel pairs of electrodes (344 individual LFP channels) within different subfields in ACC/PFC of two macaques engaged in an attention task (Fig. 1A). In the following, we report results pooled across monkeys and show that individual monkey results were consistent and qualitatively similar in SI Result S1. These recordings were from a dataset that was previously analy...

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Burst Firing Synchronizes Prefrontal and Anterior Cingulate Cortex during Attentional Control

Cited by 107 publications

References 44 publications

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice

Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice

Interareal Spike-Train Correlations of Anterior Cingulate and Dorsal Prefrontal Cortex during Attention Shifts

Theta–gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts

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