Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex

An oculomotor delayed-response task was used to examine the spatial memory functions of neurons in primate prefrontal cortex. Monkeys were trained to fixate a central spot during a brief presentation (0.5 s) of a peripheral cue and throughout a subsequent delay period (1-6 s), and then, upon the extinction of the fixation target, to make a saccadic eye movement to where the cue had been presented. Cues were usually presented in one of eight different locations separated by 45°. This task thus requires monkeys to direct their gaze to the location of a remembered visual cue, controls the retinal coordinates of the visual cues, controls the monkey's oculomotor behavior during the delay period, and also allows precise measurement of the timing and direction of the relevant behavioral responses. Recordings were obtained from 288 neurons in the prefrontal cortex within and surrounding the principal sulcus (PS) while monkeys performed this task. An additional 31 neurons in the frontal eye fields (FEF) region within and near the anterior bank of the arcuate sulcus were also studied. Of the 288 PS neurons, 170 exhibited task-related activity during at least one phase of this task and, of these, 87 showed significant excitation or inhibition of activity during the delay period relative to activity during the intertrial interval. Delay period activity was classified as directional for 79% of these 87 neurons in that significant responses only occurred following cues located over a certain range of visual field directions and were weak or absent for other cue directions. The remaining 21% were omnidirectional, i.e., showed comparable delay period activity for all visual field locations tested. Directional preferences, or lack thereof, were maintained across different delay intervals (1-6 s). For 50 of the 87 PS neurons, activity during the delay period was significantly elevated above the neuron's spontaneous rate for at least one cue location; for the remaining 37 neurons only inhibitory delay period activity was seen. Nearly all (92%) neurons with excitatory delay period activity were directional and few (8%) were omnidirectional. Most (62%) neurons with purely inhibitory delay period activity were directional, but a substantial minority (38%) was omnidirectional. Fifteen of the neurons with excitatory directional delay period activity also had significant inhibitory delay period activity for other cue directions. These inhibitory responses were usually strongest for, or centered about, cue directions roughly opposite those optimal for excitatory responses. The distribution of preferred cue locations was examined across the population of PS neurons having directional delay period activity. All possible cue locations were represented (left, right, up, down, and obliques); however, preferred cue locations in the contralateral hemifield predominated. Tuning curves were calculated by the Gaussian formula to determine the directional specificity of delay period activity. The mean tuning indices (T(d)) of PS neurons were 26.8° for excitatory delay period activity and 43.5° for inhibitory delay period activity. Delay period activity was examined on trials in which the monkey made large saccadic errors for cues in a neuron's preferred direction. Delay period activity was either truncated or absent altogether on such trials. Of the 31 FEF neurons examined, 22 exhibited task-related activity: 17 had delay period activity and 10 showed directional delay period activity. The mean tuning index (T(d)) of excitatory directional delay period activity in the FEF was 27.4°. These results indicate that prefrontal neurons (both PS and FEF) possess information concerning the location of visual cues during the delay period of the oculomotor delayed-response task. This information appears to be in a labeled line code: different neurons code different cue locations and the same neuron repeatedly codes the same location. This mnemonic activity occurs during the 1- to 6-s delay interval - in the absence of any overt stimuli or movements - and it ceases upon the execution of the behavioral response. These results strengthen the evidence that the dorsolateral prefrontal cortex participates in the process of working or transient memory and further indicate that this area of the cortex contains a complete 'memory' map of visual space.