Corollary discharge circuits for saccadic modulation of the pigeon visual system

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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.

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Figure 1: Visual structures and pathways are similar in birds and mammals.
Figure 2: Firing patterns and time course of responses in visual neurons in four brain regions during spontaneous saccades and OKN.
Figure 3: Comparisons of responses of nOPT neurons during saccades across stationary gratings and simulated saccade-like motion of gratings.
Figure 4: Effects of blockade of the optokinetic nuclei by GABA on saccadic responses of nOPT neurons.
Figure 5: Effects of optokinetic or raphe lesions on saccadic responses of thalamic and optokinetic neurons.
Figure 6: Classification of raphe neurons and their responses to antidromic stimulation of the optokinetic nuclei.
Figure 7: Responses of neurons in the nBOR and nLM to electrical stimulation of the raphe complex.
Figure 8: Summary diagram showing neuronal pathways and information flow related to saccadic responses in the structures under study (light gray rectangles; dark gray represents structures not studied here).

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Acknowledgements

We thank S.G. Lisberger of University of California San Francisco for help in editing the manuscript. This work was supported by the National Natural Science Foundation of China (90208008) and by the Chinese Academy of Sciences (KSCX1-YW-R-32 and Brain-Mind Project).

Author information

Yan Yang conducted the experiments throughout, P.C. conducted the first half of the experiments, Yang Yang conducted the second half of the experiments and S.-R.W. supervised the project and wrote the manuscript. All co-authors conducted the data analyses.

Correspondence to Shu-Rong Wang.

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