Monkey Dorsolateral Prefrontal Cortex Sends Task-Selective Signals Directly to the Superior Colliculus

Abstract

The dorsolateral prefrontal cortex (DLPFC) has been implicated in the ability to perform complex behaviors requiring the implementation of cognitive control. A central supposition of models of prefrontal function is that the DLPFC engages control by selectively modulating the activity of target structures to which it is connected, but no studies in the primate have directly investigated DLPFC output signals. Here, we recorded the activity of DLPFC neurons identified as sending a direct projection to the superior colliculus, a midbrain oculomotor structure, while monkeys performed alternating blocks of trials in which they had to look toward a flashed peripheral stimulus (prosaccades) and trials in which they had to look away from the stimulus in the opposite direction (antisaccades). We report the first direct evidence that the primate DLPFC sends task-selective signals to a target structure. This supports the notion that the DLPFC orchestrates the activity of other brain areas in accordance with task requirements.

Monkey Prefrontal Cortical Pyramidal and Putative Interneurons Exhibit Differential Patterns of Activity Between Prosaccade and Antisaccade Tasks

“…Differences in preparatory activity between prosaccade and antisaccade trials has been observed in many areas, and is thought to reflect a presetting of the oculomotor circuitry in advance of stimulus presentation to facilitate suppression of reflexive saccades (Munoz and Everling, 2004). We have previously reported that preparatory activity of corticotectal PFC neurons is greater on antisaccade than prosaccade trials (Johnston and Everling, 2006b). We speculate that the early task selectivity we observed in BS neurons could reflect changes in preparatory set that were not present in the saccade and delayed match to sample tasks used in other studies.…”

“…Based mainly on differences in activity of SC neurons during prosaccade and antisaccade tasks, Munoz and Everling proposed an accumulator model in which correct antisaccade performance depends on top-down control of SC saccade neurons by frontal cortical areas (Munoz and Everling, 2004). Direct support for this hypothesis is provided by the finding that corticotectal PFC neurons are more active on antisaccade than prosaccade trials (Johnston and Everling, 2006b). The current study indicates that not only output neurons but also interneurons in the PFC carry task-related activity.…”

“…Such an approach has also been successful in somatosensory (Mountcastle et al, 1969;Simons, 1978;McCormick et al, 1985), motor (Merchant et al, 2008), and visual cortex (Gur et al, 1999;Mitchell et al, 2007). Recently, we reported that PFC neurons showed task selectivity in a paradigm in which monkeys were required to alternate between blocks of prosaccade trials, in which they were required to generate a saccade to a flashed visual stimulus, and antisaccade trials (Hallett, 1978;Munoz and Everling, 2004), in which they were required to generate a saccade to the mirror location (Everling and DeSouza, 2005;Johnston and Everling, 2006b;Johnston et al, 2007). Here, we sought to investigate and quantify differences in task selectivity between cortical interneurons and pyramidal neurons.…”

“…We separated putative inhibitory interneurons from putative pyramidal neurons based on their extracellular action potential durations. Furthermore, we directly identified a subset of broad spiking neurons as pyramidal using antidromic identification (Johnston and Everling, 2006b). Putative interneurons were more active on prosaccade trials whereas putative pyramidal neurons preferred antisaccade trials.…”

Reduced Attentional Engagement Contributes to Deficits in Prefrontal Inhibitory Control in Schizophrenia

“…Neurophysiological studies with behaving monkeys show that excitatory input from DLPFC supports preparatory activity in the fixation zone of SC as part of this process (37). Given multiple lines of work showing DLPFC disturbances in schizophrenia, reduced input from this region to pretectal systems is a likely cause of increased errors on the antisaccade task.…”