We have explored the organization of a system within the brain of the primate whose function is to keep the cerebral cortex informed about the movements that the animal is making. This enables the brain to take into account such movements as it processes sensory input and programs sequential movement. The pathways we investigated carries information about eye movements to the cortex. In addition to the well known pathways from the frontal and parietal cortex to the superior colliculus (SC) that we have studied extensively in the last few years, there is a known anatomical pathway from the SC to the cerebral cortex. We have demonstrated the presence of this pathway functionaly by using the antidromic and orthodromic electrical stimulation techniques, and this year we have completed an analysis of the signals carried along this pathway and have tested the significance of the information carried to the cerebral cortex. We have been able to show using these stimulation techniques that the relay for this activity is the medialis dorsalis nucleus in the thalamus which is consistent with classical anatomy. The neurons in the medialis dorsalis have the characteristics of the neurons that we have previously studied in the SC. Furthermore by stimulating in medialis dorsalis and recording in the SC we can verify the SC neurons that go to the thalamus and they are the ones that have visual, visual-saccadic, and saccadic activity very similar to the neurons in medialis dorsalis. Our conclusion therefore is that we have isolated the way station on the pathway from SC to cerebral cortex, and have identified the nature of the information that the pathway is carrying. To our knowledge, this makes the medialis dorsalis the best understood relay nucleus that conveys back up to the cortex innformation about impending movements. What is the function of this information - why should the cerebral cortex be interested in it? One possibility is a classic one that was actually proposed by Descartes in his book in 1660, namely that the information is telling the brain what the eye has done. More exactly, the pathway is conveying information from the superior colliculus that an eye movement of a given direction and amplitude is about to be made. Such information has been referred to as an efference copy or a corollary discharge. But this is all hypothetical and we set out to test it by making a reversible lesion in the medialis dorsalis and determining how the monkey's behavior was altered. We did this with the monkey making saccades to visual targets and found minimal effect of the lesion. We then used a task that would require a corollary discharge; the monkey was required to make a saccade to one target and then a second one, but after both had disappeared, all in total darkness. In this case, in order to make the second saccade, the monkey would need to know where its eye was and that might depend on a corollary discharge. In this task after we made the reversible lesion of medialis dorsalis, the monkeys ability to make the second saccade was impaired. We interpret this set of results as indicating that the activity we have found in the medialis dorsalis is consistent with a corollary discharge to the cerebral cortex. We are now investigating whether the effect of this corollary discharge can be detected at the level of single neurons in the frontal eye fields.
| Berman, Rebecca A; Joiner, Wilsaan M; Cavanaugh, James et al. (2009) Modulation of presaccadic activity in the frontal eye field by the superior colliculus. J Neurophysiol 101:2934-42 |
| Wurtz, Robert H (2008) Neuronal mechanisms of visual stability. Vision Res 48:2070-89 |
| McAlonan, Kerry; Cavanaugh, James; Wurtz, Robert H (2008) Guarding the gateway to cortex with attention in visual thalamus. Nature 456:391-4 |
| Sommer, Marc A; Wurtz, Robert H (2008) Brain circuits for the internal monitoring of movements. Annu Rev Neurosci 31:317-38 |
| Sommer, Marc A; Wurtz, Robert H (2008) Visual perception and corollary discharge. Perception 37:408-18 |
| Sommer, Marc A; Wurtz, Robert H (2006) Influence of the thalamus on spatial visual processing in frontal cortex. Nature 444:374-7 |
| Nakahara, Hiroyuki; Morita, Kenji; Wurtz, Robert H et al. (2006) Saccade-related spread of activity across superior colliculus may arise from asymmetry of internal connections. J Neurophysiol 96:765-74 |
| Cavanaugh, James; Alvarez, Bryan D; Wurtz, Robert H (2006) Enhanced performance with brain stimulation: attentional shift or visual cue? J Neurosci 26:11347-58 |
| McAlonan, Kerry; Cavanaugh, James; Wurtz, Robert H (2006) Attentional modulation of thalamic reticular neurons. J Neurosci 26:4444-50 |
| Hanes, Doug P; Smith, Mitchell K; Optican, Lance M et al. (2005) Recovery of saccadic dysmetria following localized lesions in monkey superior colliculus. Exp Brain Res 160:312-25 |
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