Motor output evoked by subsaccadic stimulation of primate frontal eye fields

• Published in: Proceedings of the National Academy of Sciences - PNAS 2010-03, Vol.107 (13), p.6070-6075
• Main Authors: Corneil, Brian D, Elsley, James K, Nagy, Benjamin, Cushing, Sharon L
• Format: Article
• Language: English
• Subjects: Animals; Attention - physiology; Biological Sciences; Brain; Electromyography; Evoked Potentials, Visual; Eye movements; Eye Movements - physiology; Eye protection; Eyes; Eyes & eyesight; Head; Head movement; Head Movements - physiology; Macaca mulatta - physiology; Male; Mental stimulation; Motor ability; Motor Neurons - physiology; Muscular system; Neck; Neck Muscles - physiology; Neurons; Oculomotor Nerve - physiology; Photic Stimulation; Physiological stimulation; Saccades; Saccades - physiology; Sensory Thresholds - physiology; Visual Fields - physiology; Visual fixation; Visual Pathways - physiology
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.0911902107

In addition to its role in shifting the line of sight, the oculomotor system is also involved in the covert orienting of visuospatial attention. Causal evidence supporting this premotor theory of attention, or oculomotor readiness hypothesis, comes from the effect of subsaccadic threshold stimulation of the oculomotor system on behavior and neural activity in the absence of evoked saccades, which parallels the effects of covert attention. Here, by recording neck-muscle activity from monkeys and systematically titrating the level of stimulation current delivered to the frontal eye fields (FEF), we show that such subsaccadic stimulation is not divorced from immediate motor output but instead evokes neck-muscle responses at latencies that approach the minimal conduction time to the motor periphery. On average, neck-muscle thresholds were ~25% lower than saccade thresholds, and this difference is larger for FEF sites associated with progressively larger saccades. Importantly, we commonly observed lower neck-muscle thresholds even at sites evoking saccades [less-than or equal to]5° in magnitude, although such small saccades are not associated with head motion. Neck-muscle thresholds compare well with the current levels used in previous studies to influence behavior or neural activity through activation of FEF neurons feeding back to extrastriate cortex. Our results complement this previous work by suggesting that the neurobiologic substrate that covertly orients visuospatial attention shares this command with head premotor circuits in the brainstem, culminating with recruitment in the motor periphery.