Abstract:The capacity to rapidly adjust behavioral strategies according to changing task demands is closely associated with coordinated activity in lateral and medial prefrontal cortices. Subdivisions within prefrontal cortex are implicated to encode attentional task sets and to update changing task rules, particularly when changing task demands require top-down control. Here, we tested whether these top-down processes precede stimulus processing and constitute a preparatory attentional state that functionally couples … Show more
“…Our main finding characterized the statistical relation of two band-limited activity fluctuations comprising a narrow ∼5-to 10-Hz (peak at 7 Hz) theta band and a ∼35-to 55-Hz (peak at 40 Hz) gamma band. Previous studies have documented that a 5-to 10-Hz theta band is a widespread LFP signature in ACC/PFC that increases with specific demands to control goal-directed behavior (22)(23)(24)(25). Our study corroborates these reports (Fig.…”
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...
“…Our main finding characterized the statistical relation of two band-limited activity fluctuations comprising a narrow ∼5-to 10-Hz (peak at 7 Hz) theta band and a ∼35-to 55-Hz (peak at 40 Hz) gamma band. Previous studies have documented that a 5-to 10-Hz theta band is a widespread LFP signature in ACC/PFC that increases with specific demands to control goal-directed behavior (22)(23)(24)(25). Our study corroborates these reports (Fig.…”
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...
“…Our data extend these findings by showing that the peak frequencies of corticostriatal theta and gamma oscillations scale with movement speed. This suggests that theta and gamma oscillations are also involved in corticostriatal processing in the most basic functional domain of the corticobasal ganglia system, motor behavior (Marsden, 1982;Phillips et al, 1993;Mink, 1996;Turner and Desmurget, 2010).…”
Section: Discussionmentioning
confidence: 99%
“…The striatum is the main input structure of the basal ganglia (Alexander et al, 1986;Parent and Hazrati, 1995) and is thought to be involved in reinforcement learning and procedural memory (Bar-Gad et al, 2003;Schultz et al, 2003;Yin and Knowlton, 2006). Furthermore, the striatum also has an important role in motor behavior.…”
The corticostriatal axis is the main input stage of the basal ganglia and is crucial for their role in motor behavior. Synchronized oscillations might mediate interactions between cortex and striatum during behavior, yet direct evidence remains sparse. Here, we show that, during motor behavior, low-and high-frequency oscillations jointly couple cortex and striatum via cross-frequency interactions. We investigated neuronal oscillations along the corticostriatal axis in rats during rest and treadmill running. We found prominent theta and gamma oscillations in cortex and striatum, the peak frequencies of which scaled with motor demand. Theta and gamma oscillations were functionally coupled through phase-amplitude coupling. Furthermore, theta oscillations were phase coupled between structures. Together, local phase-amplitude coupling and corticostriatal theta phase coupling mediated the temporal correlation of gamma bursts between the cortex and striatum. The coordination of fast oscillations through coherent phase-amplitude coupling may be a general mechanism to regulate neuronal interactions along the corticostriatal axis and beyond.
“…Likewise, White et al (2013) concluded that in their fMRI-EEG study "it is likely that the frontal theta recorded currently has a medial frontal DMN [default mode network] source" (p. 2940; see also Michels et al, 2010 for a similar conclusion). Phillips et al (2014) provided direct evidence in the macaque for a role of theta-band oscillations in cognitive control, with a medial frontal source. It is unclear why the increased theta power recorded with EEG should be accompanied by reduced BOLD signal recorded with fMRI, but one possibility, supported by both theoretical and empirical arguments, is that periods of increased theta power may be accompanied by a decrease in power in higher frequencies such as gamma, and hence a net reduction in metabolic demand (Hsieh & Ranganath, 2014;Kilner et al, 2005).…”
Studies of prospective memory and other paradigms requiring participants to remember delayed intentions typically reveal a distinction between lateral and medial rostral prefrontal cortex, whereby the experimental condition yields increased signal in the former region and decreased signal in the latter. These regions comprise nodes of larger "task-positive" and "task-negative" networks that often show opposite patterns of signal change in response to diverse cognitive demands. However, it is not clear to what extent activity in these networks is A) inverse but equivalent, or B) functionally dissociable. In order to address this question, participants performed an "intention-offloading" task while undergoing fMRI. On each trial they remembered a delayed intention, which they had the opportunity to fulfill after a brief filled delay. In one condition they were required to set an external reminder of this intention, while in the other they acted without any external memory aid. Results indicated a clear functional dissociation between the two networks. Compared with a control task with no delayed intention, there was a highly significant reduction in task-negative deactivation when participants used an external memory aid. However, there was no reduction in task-positive activation. These results are consistent with previous evidence that medial rostral prefrontal cortex plays a prominent role in representing the content of delayed intentions, accompanied by a reduction in BOLD signal and potentially increased theta-band oscillatory activity. This role is no longer required once an external reminder has been created. By contrast, lateral rostral prefrontal cortex may play a content-free role, unaffected by the offloading of content into the external environment.
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