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Primate superior colliculus neurons activated by unexpected sensation

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Abstract

Midbrain superior colliculus (SC) contains a variety of neuronal types, influencing a rich spectrum of functions beyond gaze orienting. Here, we report on a novel class of SC neurons in the rhesus monkey (Macaca mulatta) that are activated by an unexpected perturbation in a goal-directed arm-movement task. One monkey subject reached for and pressed an illuminated target on a working panel upon a visual go-signal, while maintaining visual fixation elsewhere. On 50 % of trials, a task perturbation occurred—the working panel abruptly and unexpectedly moved against the subject’s hand after he pressed the target. During the performance, we recorded single SC neurons and found neurons activated exclusively for the task perturbation. These perturbation neurons were localized in the deep lateral zone of the SC, were silent during non-perturbed trials, did not appear to respond to task-irrelevant stimuli, and they had intriguingly long neuronal latencies. If the perturbation neurons’ activity relates to the hand-target contact, it may reflect the saliency of an unexpected sensation, i.e. a sensation that is not self-induced and thus cannot be predicted on a basis of the monkey’s motor program.

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Acknowledgments

This work was kindly supported by the Marie Curie Fellowship (NovoBrain Programme) and Ruhr-University Bochum Research School (AM) as well as the German Science Foundation and the Hertie Foundation (KPH). Our thanks go to Dr. Claudia Distler-Hoffmann for surgeries, histology, and for preparing Fig. 3; Margit Bronzel for animal care support; Wolfgang Kruse and Winfried Junke for computer support, and Stefan Dobers and Abdulhakim Al-Hakim for technical support.

Authors’ contribution

A.M. and K.P.H. designed the research; A.M. performed the experiments, analysed the data, and wrote the manuscript; K.P.H. edited the manuscript.

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Correspondence to Klaus-Peter Hoffmann.

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Mikulić, A., Hoffmann, KP. Primate superior colliculus neurons activated by unexpected sensation. Exp Brain Res 234, 3465–3471 (2016). https://doi.org/10.1007/s00221-016-4745-y

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