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A direct projection from superior colliculus to substantia nigra for detecting salient visual events

Abstract

Midbrain dopaminergic neurons respond to unexpected and biologically salient events, but little is known about the sensory systems underlying this response. Here we describe, in the rat, a direct projection from a primary visual structure, the midbrain superior colliculus (SC), to the substantia nigra pars compacta (SNc) where direct synaptic contacts are made with both dopaminergic and non-dopaminergic neurons. Complementary electrophysiological data reveal that short-latency visual responses in the SNc are abolished by ipsilateral lesions of the SC and increased by local collicular stimulation. These results show that the tectonigral projection is ideally located to relay short-latency visual information to dopamine-containing regions of the ventral midbrain. We conclude that it is within this afferent sensory circuitry that the critical perceptual discriminations that identify stimuli as both unpredicted and biologically salient are made.

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Figure 1: The tectonigral projection revealed by anterograde and retrograde tract tracing.
Figure 2: Axon terminals anterogradely labeled from the SC and forming synapses in SNc.
Figure 3: Tectonigral projection topography.
Figure 4: Response latencies of visual-evoked field potentials in the SC and the SNc.
Figure 5: Microinjections into the SC modulate VEPs both locally and in the SNc.
Figure 6: Effect of visual system aspiration lesions on visual evoked responses.

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Acknowledgements

This work was supported by a Fundação de Amparo à Pesquisa do Estado de São Paulo grant (97/10490-0 to E.C.), Wellcome Trust grants to P.R. (059735, 068012) and P.O. (062742), and Medical Research Council support for J.P.B. and J.B. (MRC Studentship). The authors are grateful to J. McHaffie for his comments on early drafts of the manuscript, to N. Walton for histological assistance and to P. Furness for help with data analysis.

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Correspondence to Peter Redgrave.

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Comoli, E., Coizet, V., Boyes, J. et al. A direct projection from superior colliculus to substantia nigra for detecting salient visual events. Nat Neurosci 6, 974–980 (2003). https://doi.org/10.1038/nn1113

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