Functional Architecture of Executive Control and Associated Event-Related Potentials

Medial frontal cortex enables executive control by monitoring relevant information and using it to adapt behavior. In macaques performing a saccade countermanding (stop-signal) task, we recorded EEG over and neural spiking across all layers of the supplementary eye field (SEF). We report the laminar organization of concurrently activated neurons monitoring the conflict between incompatible responses and the timing of events serving goal maintenance and executive control. We also show their relation to coincident event-related potentials (ERP). Neurons signaling response conflict were largely broad-spiking found across all layers. Neurons signaling the interval until specific task events were largely broad-spiking neurons concentrated in L3 and L5. Neurons predicting the duration of control and sustaining the task goal until the release of operant control were a mix of narrow- and broad-spiking neurons confined to L2/3. We complement these results with the first report of a monkey homologue of the N2/P3 ERP complex associated with response inhibition. N2 polarization varied with error likelihood and P3 polarization varied with the duration of expected control. The amplitude of the N2 and P3 were predicted by the spike rate of different classes of neurons located in L2/3 but not L5/6. These findings reveal important, new features of the cortical microcircuitry supporting executive control and producing associated ERP.

Cortical Microcircuitry of Executive Control and Source of Associated Event-Related Potentials

Medial frontal cortex enables executive control by signaling conflict, monitoring and predicting events and outcomes, and goal maintenance, indexed by event-related potentials (ERP). In monkeys performing a saccade countermanding (stop-signal) task, we recorded EEG over and neural spiking across all layers of the supplementary eye field (SEF). Neurons did not contribute to reactive response inhibition. Those signaling response conflict and tracking and predicting the timing of events for successful stopping had different spike widths and were concentrated differently across layers. Conflict neurons were in all layers and those encoding temporal parameters were concentrated in L2/3 and L5. The N2 indexed reward association with variation of polarization predicted by conflict and event timing neurons in L2/3 but not L5/6. The P3 indexed the timing of the upcoming event with variation of polarization predicted by event timing neurons in L2/3 but not L5/6. These findings reveal novel features of the cortical microcircuitry supporting executive control and producing associated ERP.

The Supplementary Eye Field Tracks Cognitive Efforts

ABSTRACTPupil dilation is known to be an index of cognitive effort. Nevertheless, our lack of knowledge of the precise dynamics through which pupil size and activity of the medial prefrontal cortex are conjugated during cognitive tasks highlights the need for its further investigation before, during, and after changes in pupil size. Here, we tested whether pupil dynamics are related to the activity of the supplementary eye field (SEF) during a mixed pro/anti-saccade oculomotor task in two macaque monkeys. We used functional ultrasound imaging (fUS) to examine temporal changes in brain activity at the 0.1-s time scale and 0.1-mm spatial resolution in relation to behavioral performance and pupil dynamics. By combining the pupil signals and real-time imaging of NHP during cognitive tasks, we were able to infer localized CBV responses within a restricted part of the dorsomedial prefrontal cortex, referred to as the SEF, an area in which anti-saccade preparation activity is also recorded. Inversely, SEF neurovascular activity measured by fUS imaging was found to be a robust predictor of specific variations in pupil diameter over short and long time scales. Furthermore, we directly manipulated pupil diameter and CBV in the SEF using reward and cognitive effort. These results demonstrate that the SEF is an underestimated but pivotal cortical area for the monitoring and implementation of cognitive effort signals.

Performance Monitoring during Visual Priming

Repetitive performance of single-feature (efficient or pop-out) visual search improves RTs and accuracy. This phenomenon, known as priming of pop-out, has been demonstrated in both humans and macaque monkeys. We investigated the relationship between performance monitoring and priming of pop-out. Neuronal activity in the supplementary eye field (SEF) contributes to performance monitoring and to the generation of performance monitoring signals in the EEG. To determine whether priming depends on performance monitoring, we investigated spiking activity in SEF as well as the concurrent EEG of two monkeys performing a priming of pop-out task. We found that SEF spiking did not modulate with priming. Surprisingly, concurrent EEG did covary with priming. Together, these results suggest that performance monitoring contributes to priming of pop-out. However, this performance monitoring seems not mediated by SEF. This dissociation suggests that EEG indices of performance monitoring arise from multiple, functionally distinct neural generators.

Neural Mechanisms for Executive Control of Speed-Accuracy Tradeoff

SUMMARYThe balance of speed with accuracy requires error detection and performance adaptation. To date, neural concomitants of these processes have been investigated only with noninvasive measures. To provide the first neurophysiological description, macaque monkeys performed visual search under cued speed accuracy tradeoff (SAT). Monkeys changed SAT emphasis immediately after a cued switch while neuron discharges were sampled in medial frontal cortex area supplementary eye field (SEF). A multiplicity of SEF neurons signaled production of choice errors and timing errors. Modulation of SEF activity after choice errors predicted production of un-rewarded corrective saccades. Modulation of activity after timing errors signaled reward prediction error. Adaptation of performance during SAT of visual search was accomplished through pronounced changes in neural state from before search array presentation until after reward delivery. These results contextualize previous findings using noninvasive measures, complement neurophysiological findings in visuomotor structures, endorse the role of medial frontal cortex as a critic relative to the actor instantiated in visuomotor structures, and extend our understanding of the distributed neural mechanisms of SAT.HIGHLIGHTSMedial frontal cortex enables post-error adjustment during SATChoice and timing errors were signaled by partially overlapping neural poolsMedial frontal cortex can proactively modulate visuomotor processesMedial frontal cortex is to visuomotor circuits as critic to actor