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...

Short periods of oscillatory activation are ubiquitous signatures of neural circuits. A broad range of studies documents not only their circuit origins, but also a fundamental role for oscillatory activity in coordinating information transfer during goal directed behavior. Recent studies suggest that resetting the phase of ongoing oscillatory activity to endogenous or exogenous cues facilitates coordinated information transfer within circuits and between distributed brain areas. Here, we review evidence that pinpoints phase resetting as a critical marker of dynamic state changes of functional networks. Phase resets: (1) set a “neural context” in terms of narrow band frequencies that uniquely characterizes the activated circuits; (2) impose coherent low frequency phases to which high frequency activations can synchronize, identifiable as cross-frequency correlations across large anatomical distances; (3) are critical for neural coding models that depend on phase, increasing the informational content of neural representations; and (4) likely originate from the dynamics of canonical E-I circuits that are anatomically ubiquitous. These multiple signatures of phase resets are directly linked to enhanced information transfer and behavioral success. We survey how phase resets re-organize oscillations in diverse task contexts, including sensory perception, attentional stimulus selection, cross-modal integration, Pavlovian conditioning, and spatial navigation. The evidence we consider suggests that phase-resets can drive changes in neural excitability, ensemble organization, functional networks, and ultimately, overt behavior.

This document describes the tests performed to characterize USE system latencies relating to the USE I/O Box. Test methods and results are summarized.

Population-level theta and beta band activity in anterior cingulate and prefrontal cortices (ACC/PFC) are prominent signatures of self-controlled, adaptive behaviors. But how these rhythmic activities are linked to cell-type specific activity has remained unclear. Here, we suggest such a cell-to-systems level linkage. We found that the rate of burst spiking events is enhanced particularly during attention states and that attention-specific burst spikes have a unique temporal relationship to local theta and beta band population-level activities. For the 5-10 Hz theta frequency range, bursts coincided with transient increases of local theta power relative to nonbursts, particularly for bursts of putative interneurons. For the 16-30 Hz beta frequency, bursts of putative interneurons phase synchronized stronger than nonbursts, and were associated with larger beta power modulation. In contrast, burst of putative pyramidal cells showed similar beta power modulation as nonbursts, but were accompanied by stronger beta power only when they occurred early in the beta cycle. These findings suggest that in the ACC/PFC during attention states, mechanisms underlying burst firing are intimately linked to narrow band population-level activities, providing a cell-type specific window into rhythmic inhibitory gating and the emergence of rhythmically coherent network states during goal directed behavior.

Many studies of vision and cognition require novel three-dimensional object sets defined by a parametric feature space. Creating such sets and verifying that they are suitable for a given task, however, can be time-consuming and effortful. Here we present a new set of multidimensional objects, Quaddles, designed for studies of feature-based learning and attention, but adaptable for many research purposes. Quaddles have features that are all equally visible from any angle around the vertical axis and can be designed to be equally discriminable along feature dimensions; these objects do not show strong or consistent response biases, with a small number of quantified exceptions. They are available as two-dimensional images, rotating videos, and FBX object files suitable for use with any modern video game engine. We also provide scripts that can be used to generate hundreds of thousands of further Quaddles, as well as examples and tutorials for modifying Quaddles or creating completely new object sets from scratch, with the aim to speed up the development time of future novel-object studies.

Saccade detection is a critical step in the analysis of gaze data. A common method for saccade detection is to use a simple threshold for velocity or acceleration values, which can be estimated from the data using the mean and standard deviation. However, this method has the downside of being influenced by the very signal it is trying to detect, the outlying velocities or accelerations that occur during saccades. We propose instead to use the median absolute deviation (MAD), a robust estimator of dispersion that is not influenced by outliers. We modify an algorithm proposed by Nyström and colleagues, and quantify saccade detection performance in both simulated and human data. Our modified algorithm shows a significant and marked improvement in saccade detection - showing both more true positives and less false negatives – especially under higher noise levels. We conclude that robust estimators can be widely adopted in other common, automatic gaze classification algorithms due to their ease of implementation.

The prefrontal cortex and striatum form a recurrent network whose spiking activity encodes multiple types of learning-relevant information. This spike-encoded information is evident in average firing rates, but finer temporal coding might allow multiplexing and enhanced readout across the connected network. We tested this hypothesis in the fronto-striatal network of nonhuman primates during reversal learning of feature values. We found that populations of neurons encoding choice outcomes, outcome prediction errors, and outcome history in their firing rates also carry significant information in their phase-of-firing at a 10–25 Hz band-limited beta frequency at which they synchronize across lateral prefrontal cortex, anterior cingulate cortex and anterior striatum when outcomes were processed. The phase-of-firing code exceeds information that can be obtained from firing rates alone and is evident for inter-areal connections between anterior cingulate cortex, lateral prefrontal cortex and anterior striatum. For the majority of connections, the phase-of-firing information gain is maximal at phases of the beta cycle that were offset from the preferred spiking phase of neurons. Taken together, these findings document enhanced information of three important learning variables at specific phases of firing in the beta cycle at an inter-areally shared beta oscillation frequency during goal-directed behavior.

To navigate, we must represent information about our place in the environment. Traditional research highlights the role of the hippocampal complex in this process. Spurred by recent research highlighting the widespread cortical encoding of cognitive and motor variables previously thought to have localized function, we hypothesized that navigational variables would be likewise encoded widely, especially in the prefrontal cortex, which is often associated with control of volitional behavior. We recorded neural activity from six prefrontal structures while macaques performed a foraging task in an open enclosure. In all six regions, we found strong encoding of allocentric position, head direction, egocentric boundary distance, and linear and angular velocity. These encodings were not accounted for by distance or time to reward. Strength of coding of all variables increase along a ventral-to-dorsal gradient. Together these results argue that encoding of navigational variables is not localized to the hippocampal complex and support the hypothesis that navigation is continuous with other forms of flexible cognition in the service of action.