Predictive responses of periarcuate pursuit neurons to visual target motion

• Published in: Experimental brain research 2002-07, Vol.145 (1), p.104-120
• Main Authors: FUKUSHIMA, Kikuro, YAMANOBE, Takanobu, SHINMEI, Yasuhiro, FUKUSHIMA, Junko
• Format: Article
• Language: English
• Subjects: Action Potentials - physiology; Animals; Biological and medical sciences; cortex (periarcuate); Eye and associated structures. Visual pathways and centers. Vision; Eye movements; Feedback; Fixation, Ocular - physiology; Frontal Lobe - cytology; Frontal Lobe - physiology; Fundamental and applied biological sciences. Psychology; Macaca - anatomy & histology; Macaca - physiology; Macaca fuscata; Male; Monkeys & apes; Motion Perception - physiology; Neurons - cytology; Neurons - physiology; Photic Stimulation; Psychomotor Performance - physiology; Pursuit, Smooth - physiology; Reaction Time - physiology; Velocity; Vertebrates: nervous system and sense organs; Visual Pathways - cytology; Visual Pathways - physiology
• ISSN: 0014-4819; 1432-1106
• DOI: 10.1007/s00221-002-1088-7

The smooth pursuit eye movement system uses retinal information about the image-slip-velocity of the target in order to match the eye-velocity-in-space (i.e., gaze-velocity) to the actual target velocity. To maintain the target image on the fovea during smooth gaze tracking, and to compensate for the long delays involved in processing visual motion information and/or eye velocity commands, the pursuit system must use prediction. We have shown recently that both retinal image-slip-velocity and gaze-velocity signals are coded in the discharge of single pursuit-related neurons in the simian periarcuate cortex. To understand how periarcuate pursuit neurons are involved in predictive smooth pursuit, we examined the discharge characteristics of these neurons in trained Japanese macaques. When a stationary target abruptly moved sinusoidally along the preferred direction at 0.5 Hz, the response delays of pursuit cells seen at the onset of target motion were compensated in succeeding cycles. The monkeys were also required to continue smooth pursuit of a sinusoidally moving target while it was blanked for about half of a cycle at 0.5 Hz. This blanking was applied before cell activity normally increased and before the target changed direction. Normalized mean gain of the cells' responses (re control value without blanking) decreased to 0.81(+/-0.67 SD), whereas normalized mean gain of the eye movement (eye gain) decreased to 0.65 (+/-0.16 SD). A majority (75%) of pursuit neurons discharged appropriately up to 500 ms after target blanking even though eye velocity decreased sharply, suggesting a dissociation of the activity of those pursuit neurons and eye velocity. To examine whether pursuit cell responses contain a predictive component that anticipates visual input, the monkeys were required to fixate a stationary target while a second test laser spot was moved sinusoidally. A majority (68%) of pursuit cells tested responded to the second target motion. When the second spot moved abruptly along the preferred direction, the response delays clearly seen at the onset of sinusoidal target motion were compensated in succeeding cycles. Blanking (400-600 ms) was also applied during sinusoidal motion at 1 Hz before the test spot changed its direction and before pursuit neurons normally increased their activity. Preferred directions were similar to those calculated for target motion (normalized mean gain=0.72). Similar responses were also evoked even if the second spot was fl