Unit study of monkey frontal cortex: Active localization of auditory and of visual stimuli

1. The influence of sound localization behavior on unit activity in the frontal cortex of awake rhesus monkeys was examined by comparing responses under three behavioral conditions: 1) auditory localization, during which a response was required to the location of a sound (broad-band noise) source; 2) auditory detect, during which a response was required to indicate the occurrence of the sound regardless of location; 3) visual localization, during which no sounds were presented and a response was required to the location of a visual stimulus; and 4) nonperform, presentation of auditory stimuli as in the first two conditions, but with the animal sitting passively. 2. Extracellular microelectrode recordings were made in the periarcuate (10) region and dorsal and ventral prefrontal areas near the principal sulcus. Four monkeys were used with a total of 498 cells studied. 3. Of the total population, only five cells were found to have characteristics similar to those of auditory units in the primary auditory cortex and the surrounding belt area (7). More typically, units were found that had strong short-latency responses specific to the auditory and/or visual localization tasks. These units had no or weak responses when the same sound stimuli were presented in the auditory detect task or when a monkey received the sound stimuli in a nonperforming condition. 4. Two regions were identified, one medial and/or posterior to the arcuate sulcus, in Brodmann's (8) area 6; the second included parts of areas 8 and 9 within the genu of the arcuate sulcus. Units from these regions are referred to, respectively, as the postarcuate and the prearcuate populations. Both populations responded predominantly during active localization behavior. Sixty-two percent of the postarcuate population responded during auditory localization, 32% responded during auditory detect, and only 18% responded to acoustic stimuli presented in the nonperforming condition. In the prearcuate population percentages in these three conditions were 35, 25, and 12%, respectively. For visual localization, 54% in the postarcuate population responded, whereas 42% in the prearcuate responded. 5. Spatial tuning of units during auditory localization was similar to that seen in units of the primary auditory cortex (7), with the greatest percentages of units responding to stimuli contralateral to the recording site. Similar tuning was observed for the visual localization task as well. 6. Similarities in spatial tuning between the auditory and visual localization conditions were examined to assess the 'bimodal' nature of the units. Units with a high degree of similarity in spatial tuning for the auditory and visual localization conditions and with dissimilar tuning for the detect condition were candidates to be considered 'localization-specific' units. In the postarcuate population, 36% of the units were localization specific, whereas only 12% of the prearcuate units had this property. 7. In the primary auditory cortex and belt areas of the superior temporal plane nearly all units were responsive to sound (7). In the frontal regions of the present study, a variety of response types were noted including early, late, prestimulus, and inhibitory responses. Further, some units encountered and studied had no response at all. Twenty percent of the postarcuate population and 32% of the prearcuate population were in this category. 8. The majority of units studied did not have responses synchronized with either arm movements made in the execution of motor responses or eye movements to target locations. A substantial proportion of the units studied appear to be involved in active localization of stimuli in the external environment. There were a few units with dual function, localization as well as motor, as reflected in their early and late activity.