Functional and behavioral effects induced by electrical microstimulation of monkey FEF during selective spatial attention tasks

Abstract

Several studies provided evidence for a prominent role of the frontal eye fields (FEF) in the allocation of attention. FEF is an area of the frontal cortex involved in linking visual information with saccade commands and is thought to modulate incoming sensory signals through feedback signals. For example, Moore and Fallah (2004) have shown that electrical microstimulation of macaque FEF (FEF-EM) increases performance for stimuli presented inside the stimulated movement field (MF) in a luminance contrast detection task. In a separate study, Moore and Armstrong (2003) also showed that FEF-EM enhances neural activity to visual stimuli in retinotopically corresponding sites in area V4 in a similar fashion to attention. A subsequent pharmacological study by Noudoost and Moore (2011) was able to identify dopamine D1 receptors in FEF as mediating prefrontal control of visual cortical signals. Ekstrom et al. (2008, 2009), on the other hand, showed that FEF-EM most strongly enhanced fMRI activity in voxels of visual cortex that were located adjacent to the voxels with the strongest visual response. Voxels activated strongest by a visual stimulus were unaffected or even suppressed by concurrent FEF-EM. In an attempt to directly link behavioral with functionally FEF-EM triggered effects in the same experiment, we chronically implanted 25 micron Pt/Ir micro-wires for FEF-EM in two monkeys performing a selective spatial attention task. The monkeys were trained to indicate the orientation of a peripherally presented low-contrast grating stimulus at threshold level while ignoring a similar grating stimulus in the opposite hemifield. Unilateral FEF-EM slightly decreased the monkey’s performance in this task. Given this surprising result, we also trained our monkeys on exactly the same contrast detection task as used by Moore and Fallah (2004). We ran 117 experiments at 20 different electrode positions in two monkeys. Out of these 20 sites 11 sites did not reveal any significant effect of FEF-EM on contrast detection thresholds for stimuli presented in the center of the MF. Only three sites showed a significant positive effect and 6 sites showed a significant negative effect on performance. Concurrent fMRI - FEF-EM experiments using the same tasks revealed inhibition of activity in early visual areas at the retinotopic location of the visual stimuli. Our data are in line with the passive viewing results from Ekstrom et al. (2008) and suggest that both suppressive and enhancement signals may be transmitted from FEF to occipital cortex.status: publishe