Our mental activity is internal and not directly observable, but we can infer much about it by measuring what we perceive and how we move. For the rapid eye movements we make several times per second, the need for such internal monitoring has been recognized at least since Descartes in the 17th century. Sperry and von Holst and Middlestadt experimentally demonstrated the need for these internal signals in the 20th century and referred to the signals as corollary discharge or efference copy. In the monkey a circuit for such a corollary discharge for rapid or saccadic eye movements has recently been found;it extends from the superior colliculus in the brain stem, through the medial dorsal nucleus of the thalamus, to the frontal eye field of frontal cortex (Sommer and Wurtz, 2002, 2006). This corollary discharge pathway can be interrupted in the thalamus by reversible inactivation, and such interruption has revealed two contributions of the corollary discharge. First, the corollary signal enables frontal cortex to generate rapid sequential eye movements without direct visual guidance, a feat essential for skilled athletic performance. Second, the corollary is likely to be critical for maintaining our perception of a stable visual world in spite of incessant eye movements. Many frontal eye field neurons receive an anticipatory input indicating that the visual information they are about to receive results from the moving eye rather than from a moving environment (Duhamel, Colby, and Goldberg, 1992). Inactivation of this pathway reduces this anticipatory activity, and along with other characteristics of these frontal cortex neurons, suggests that their activity is part of the mechanism underlying visual stability. While these experiments have concentrated on just eye movements, and just one pathway to cortex, they may provide a model for investigating the multiple ascending pathways through thalamus to all regions of cortex, which monitor not only movement but the multiple functions the brain performs. We have now investigated the role of attention in modifying the anticipatory response in the monkey frontal eye field (FEF) region of the frontal cortex. We first verified that the sensitivity of some neurons to visual stimulation changes just before the onset of a saccade. It shifts from the location of its current receptive field (RF) to the location of that field after the saccade is completed (the future field, FF). We have now investigated whether the shift also depends on the monkeys visual attention. In the standard experiment, there is only one stimulus on an otherwise empty visual field, and this probably produces a strong onset attention effect. In the present experiments we compared the magnitude of the shift effect when there was only one visual stimulus to the case where there were multiple visual stimuli. We studied neurons that showed a shift effect and first determined the size of their RF. We then determined neuronal activity when in addition to the single stimulus flashed in the FF just before the saccade, we flashed multiple distractor stimuli at the same time. These distractors fell outside of the mapped RF before and after the saccade. If the FF activity of a neuron were facilitated by onset attention, we expected to see a reduction in the FF activity when multiple stimuli were presented which should reduce the onset attention effect. FF activity was reduced in many neurons. We conclude that attention is a key contributing factor to the strength of the shifting receptive field activity in the FEF. This suggests that the shifting RF mechanism need not apply to the entire visual field with each saccade but only to those regions to which attention is directed. The finding provides further support for the emerging view that our perception is not of the whole visual field but only of that sub-region to which we attend.
| Cavanaugh, James; Berman, Rebecca A; Joiner, Wilsaan M et al. (2016) Saccadic Corollary Discharge Underlies Stable Visual Perception. J Neurosci 36:31-42 |
| Wurtz, Robert H (2015) Using perturbations to identify the brain circuits underlying active vision. Philos Trans R Soc Lond B Biol Sci 370: |
| Joiner, Wilsaan M; Cavanaugh, James; Wurtz, Robert H (2013) Compression and suppression of shifting receptive field activity in frontal eye field neurons. J Neurosci 33:18259-69 |
| Wurtz, Robert H (2013) Retrospective. David H. Hubel (1926-2013). Science 342:572 |
| Joiner, Wilsaan M; Cavanaugh, James; FitzGibbon, Edmond J et al. (2013) Corollary discharge contributes to perceived eye location in monkeys. J Neurophysiol 110:2402-13 |
| Cavanaugh, James; Monosov, Ilya E; McAlonan, Kerry et al. (2012) Optogenetic inactivation modifies monkey visuomotor behavior. Neuron 76:901-7 |
| Cavanaugh, James; Joiner, Wilsaan M; Wurtz, Robert H (2012) Suppressive surrounds of receptive fields in monkey frontal eye field. J Neurosci 32:12284-93 |
| Berman, Rebecca A; Wurtz, Robert H (2011) Signals conveyed in the pulvinar pathway from superior colliculus to cortical area MT. J Neurosci 31:373-84 |
| Wurtz, Robert H; McAlonan, Kerry; Cavanaugh, James et al. (2011) Thalamic pathways for active vision. Trends Cogn Sci 15:177-84 |
| Joiner, Wilsaan M; Cavanaugh, James; Wurtz, Robert H (2011) Modulation of shifting receptive field activity in frontal eye field by visual salience. J Neurophysiol 106:1179-90 |
Showing the most recent 10 out of 17 publications
