Cell-Type-Specific Synchronization of Neural Activity in FEF with V4 during Attention

Gregoriou, Georgia G.; Gotts, Stephen J.; Desimone, Robert

doi:10.1016/j.neuron.2011.12.019

Cited by 217 publications

(203 citation statements)

References 74 publications

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“…The cortical ACC/PFC fields engaging in theta-locked low-gamma activation in our study anatomically connect to the FEF. This makes it likely that the thetaphase reset we observed in ACC/PFC also synchronizes FEF gamma-activity bursts and spiking activity of visually selective FEF neurons that most strongly synchronize to the local, lowgamma activity in FEF during sustained selective attentional processing (34). We can thus speculate that the band-limited neuronal activation of the specific theta and gamma bands that interact during attention shifts in our study may serve as general band-limited signatures of neuronal coordination of attention information during goal-directed behaviors.…”

Section: Discussionmentioning

confidence: 85%

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.

135

129

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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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Section: Discussionmentioning

confidence: 85%

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.

135

129

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“…Our results indicate that these two roles might not be mutually exclusive. The gamma activity raised in power in a time frame that was much later than the initial visual response period in sensory-motor regions including FEF (33) and LIP (21) but also much earlier than the saccade epoch and, therefore, may represent an important intermediate step of visual selection that precedes saccades.…”

Section: Discussionmentioning

confidence: 99%

Simultaneous analysis of the LFP and spiking activity reveals essential components of a visuomotor transformation in the frontal eye field

Sendhilnathan

Basu

Murthy

2017

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

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The frontal eye field (FEF) is a key brain region to study visuomotor transformations because the primary input to FEF is visual in nature, whereas its output reflects the planning of behaviorally relevant saccadic eye movements. In this study, we used a memory-guided saccade task to temporally dissociate the visual epoch from the saccadic epoch through a delay epoch, and used the local field potential (LFP) along with simultaneously recorded spike data to study the visuomotor transformation process. We showed that visual latency of the LFP preceded spiking activity in the visual epoch, whereas spiking activity preceded LFP activity in the saccade epoch. We also found a spatially tuned elevation in gamma band activity (30-70 Hz), but not in the corresponding spiking activity, only during the delay epoch, whose activity predicted saccade reaction times and the cells' saccade tuning. In contrast, beta band activity (13-30 Hz) showed a nonspatially selective suppression during the saccade epoch. Taken together, these results suggest that motor plans leading to saccades may be generated internally within the FEF from local activity represented by gamma activity.T he process of generating a motor plan from visual information entails a visuomotor transformation. The frontal eye field (FEF) is one of the cortical regions that contributes to the visuomotor transformation process by participating in critical events such as target selection (1-3) and saccade preparation (4-6). In addition to FEF, other oculomotor areas such as the lateral intraparietal cortex (7), the supplementary eye fields (8), the superior colliculus (9), and the dorsolateral prefrontal cortex (10) also possess neurons with similar properties as FEF neurons. Thus, a central question that remains unresolved is to what extent do the response properties of FEF neurons represent a cause versus a consequence of computations occurring elsewhere.One approach to resolve this question of causation versus consequence, in the context of target selection, was the use of simultaneously recorded local field potentials (LFP) and spikesmaking use of the idea that the LFP represents synchronized input coming into a brain area, as opposed to spiking activity, which is thought to represent output (11)(12)(13)(14)(15). Using this approach, Monosov et al. showed that FEF received spatially nonselective input through LFP earlier than spikes in the early visual epoch; however, in the consequent target selection epoch, spiking activity of FEF neurons evolved spatial selectivity and actively discriminated between the behaviorally relevant and the irrelevant stimuli earlier than the LFP (1). Such a temporal relationship between LFP and spikes during target selection in FEF has also been studied by others using simultaneously recorded LFP and spikes, converging to the same evidence (5, 16). However, whereas these studies suggest a causal role for FEF in visual selection, the causal role of FEF in saccade preparation has not yet been reported. In this study, we asked whether sac...

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“…Specifically, several visuomotor areas play crucial roles in both the deployment of visual attention and the generation of saccades, including the frontal eye field (FEF) and lateral intraparietal area (LIP), as well as the superior colliculus (SC) at the subcortical level (Awh et al 2006;Moore 2006;Bisley 2011;Krauzlis et al 2013), with a division of labor at the level of neural subpopulations (Ignashchenkova et al 2004;Juan et al 2004;Thompson et al 2005;Gregoriou et al 2012). Using functional MRI in humans, Culham et al (1998) showed that attentive tracking of moving objects activated FEF and the intraparietal sulcus (IPS; the human homologue of LIP) more than twice as much as passive viewing of the same stimuli.…”

Section: Discussionmentioning

confidence: 99%

Attentional trade-offs maintain the tracking of moving objects across saccades

Szinte

Carrasco

Cavanagh

et al. 2015

Journal of Neurophysiology

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Cell-Type-Specific Synchronization of Neural Activity in FEF with V4 during Attention

Cited by 217 publications

References 74 publications

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

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

Simultaneous analysis of the LFP and spiking activity reveals essential components of a visuomotor transformation in the frontal eye field

Attentional trade-offs maintain the tracking of moving objects across saccades

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