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J Neurophysiol 91: 1381-1402, 2004. First published October 22, 2003; doi:10.1152/jn.00738.2003
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What the Brain Stem Tells the Frontal Cortex. I. Oculomotor Signals Sent From Superior Colliculus to Frontal Eye Field Via Mediodorsal Thalamus

Marc A. Sommer and Robert H. Wurtz

Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892-4435

Submitted 31 July 2003; accepted in final form 24 September 2003

Neuronal processing in cerebral cortex and signal transmission from cortex to brain stem have been studied extensively, but little is known about the numerous feedback pathways that ascend from brain stem to cortex. In this study, we characterized the signals conveyed through an ascending pathway coursing from the superior colliculus (SC) to the frontal eye field (FEF) via mediodorsal thalamus (MD). Using antidromic and orthodromic stimulation, we identified SC source neurons, MD relay neurons, and FEF recipient neurons of the pathway in Macaca mulatta. The monkeys performed oculomotor tasks, including delayed-saccade tasks, that permitted analysis of signals such as visual activity, delay activity, and presaccadic activity. We found that the SC sends all of these signals into the pathway with no output selectivity, i.e., the signals leaving the SC resembled those found generally within the SC. Visual activity arrived in FEF too late to contribute to short-latency visual responses there, and delay activity was largely filtered out in MD. Presaccadic activity, however, seemed critical because it traveled essentially unchanged from SC to FEF. Signal transmission in the pathway was fast (~2 ms from SC to FEF) and topographically organized (SC neurons drove MD and FEF neurons having similarly eccentric visual and movement fields). Our analysis of identified neurons in one pathway from brain stem to frontal cortex thus demonstrates that multiple signals are sent from SC to FEF with presaccadic activity being prominent. We hypothesize that a major signal conveyed by the pathway is corollary discharge information about the vector of impending saccades.


Address for reprint requests and other correspondence: M. A. Sommer, Bldg 49, Room 2A50, MSC 4435, NEI, NIH, 9000 Rockville Pike, Bethesda, MD 20892-4435 (E-mail: mas{at}lsr.nei.nih.gov).




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