Corollary discharge circuits for saccadic modulation of the pigeon visual system

Abstract

A saccadic eye movement causes a variety of transient perceptual sequelae that might be the results of corollary discharge. Here we describe the neural circuits for saccadic corollary discharge that modulates activity throughout the pigeon visual system. Saccades in pigeons caused inhibition that was mediated by corollary discharge followed by enhancement of firing activity in the telencephalic hyperpallium, visual thalamus and pretectal nucleus lentiformis mesencephali (nLM) with opposite responses in the accessory optic nucleus (nBOR). Inactivation of thalamic neurons eliminated saccadic responses in telencephalic neurons, and inactivation of both the nLM and the nBOR abolished saccadic responses in thalamic neurons. Saccade-related omnipause neurons in the brainstem raphe complex inhibited the nBOR and excited the nLM, whereas inactivation of raphe neurons eliminated saccadic responses in both optokinetic and thalamic neurons. It seems that saccadic responses in telencephalic neurons are generated by corollary discharge signals from brainstem neurons that are transmitted through optokinetic and thalamic neurons. These signals might have important roles in visual perception.

Neuronal Circuitry and Discharge Patterns Controlling Eye Movements in the Pigeon

“…They were divided into three groups for experimentation. The first group included 41 pigeons, each of which was anesthetized by injection of a mixture of ketamine (40 mg/Kg) and xylazine (5 mg/Kg) into pectoral muscles (Wang et al, 1995;Yang et al, 2008), and the depth of anesthesia was monitored by breathing patterns and by the reflex from pinching the toe. The pigeon was then placed in a stereotaxic apparatus and its scalp was incised and retracted, and the caudal tectum and cerebellum were exposed with a dental drill and surgical forceps.…”

“…It then was lightly anesthetized with ketamine and xylazine and wrapped in a bag and placed on a foam couch in the stereotaxic apparatus. Its headpiece was reconnected to the rod for stereotaxic fixation, and the wound edge and muscles were infiltrated periodically with lidocaine (Yang et al, 2008). The dura mater overlying the right abducens nucleus and that overlying the left oculomotor nucleus were excised and the brain surface covered with liquid paraffin.…”

“…A tangent screen of 130°vertical by 140°horizontal was placed 40 cm away from the viewing eye. The horizontal axis of the visual field on the screen was rotated by 38°to match the pigeon's normal conditions (Cao et al, 2004;Niu et al, 2006;Li et al, 2007;Yang et al, 2008).…”

“…Action potentials were amplified, displayed and stored in a digital data recorder (RD-135T; TEAC) for off-line analysis. (2) Twobarrel micropipettes (5-10 m in diameter) were used for blocking nBOR/nLM or the raphe complex, one barrel of which was filled with 2 M sodium acetate and 2% pontamine sky blue to physiologically and anatomically confirm the electrode tip location, and the other contained GABA (100 mM, pH 3.3) or kainic acid (9.4 mM, pH 7.4; Sigma) and was connected to a pneumatic picopump (PV800; World Precision Instruments) for applying GABA (0.08 -0.12 l) or kainic acid (0.2-0.3 l) (Gioanni et al, 1983;Gu et al, 2001;Cao et al, 2006;Yang et al, 2008). (3) A tungsten bipolar electrode was used for electrical stimulation of the left oculomotor nucleus and for electrolytic lesions of nLM/nBOR or the raphe complex as well.…”

“…In this respect, the oculomotor system in birds may provide a good model to explore these problems (Yang et al, 2008) because avian saccade consists of a shift of eye position and several cycles of oscillation (Wallman et al, 1994;Niu et al, 2006;Yang et al, 2008), and these saccadic components may originate from different neural structures. Recent studies found two types of omnipause neurons in the brainstem raphe complex, which project to the nucleus of the basal optic root (nBOR) (Toledo et al, 1995;Yang et al, 2008) and the nucleus lentiformis mesencephali (nLM) (Yang et al, 2008). Together with the fact that the raphe complex receives afferents from the optic tectum (Hunt and Kü nzle, 1976;Reiner and Karten, 1982;Luksch, 2003), it suggests that the raphe complex may be involved in generating saccades.…”