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The Journal of Neurophysiology Vol. 87 No. 2 February 2002, pp. 845-858
Copyright ©2002 by the American Physiological Society
Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892
Ferraina, Stefano,
Martin Paré, and
Robert H. Wurtz.
Comparison of Cortico-Cortical and Cortico-Collicular Signals for
the Generation of Saccadic Eye Movements. J. Neurophysiol. 87: 845-858, 2002. Many
neurons in the frontal eye field (FEF) and lateral intraparietal (LIP)
areas of cerebral cortex are active during the visual-motor events
preceding the initiation of saccadic eye movements: they respond to
visual targets, increase their activity before saccades, and maintain
their activity during intervening delay periods. Previous experiments
have shown that the output neurons from both LIP and FEF convey the
full range of these activities to the superior colliculus (SC) in the
brain stem. These areas of cerebral cortex also have strong
interconnections, but what signals they convey remains unknown. To
determine what these cortico-cortical signals are, we identified the
LIP neurons that project to FEF by antidromic activation, and we
studied their activity during a delayed-saccade task. We then compared
these cortico-cortical signals to those sent subcortically by also
identifying the LIP neurons that project to the intermediate layers of
the SC. Of 329 FEF projection neurons and 120 SC projection neurons,
none were co-activated by both FEF and SC stimulation. FEF projection neurons were encountered more superficially in LIP than SC projection neurons, which is consistent with the anatomical projection of many
cortical layer III neurons to other cortical areas and of layer V
neurons to subcortical structures. The estimated conduction velocities
of FEF projection neurons (16.7 m/s) were significantly slower that
those of SC projection neurons (21.7 m/s), indicating that FEF
projection neurons have smaller axons. We identified three main
differences in the discharge properties of FEF and SC projection
neurons: only 44% of the FEF projection neurons changed their activity
during the delayed-saccade task compared with 69% of the SC projection
neurons; only 17% of the task-related FEF projection neurons showed
saccadic activity, whereas 42% of the SC projection neurons showed
such increases; 78% of the FEF projection neurons had a visual
response but no saccadic activity, whereas only 55% of the SC
projection neurons had similar activity. The FEF and SC projection
neurons had three similarities: both had visual, delay, and saccadic
activity, both had stronger delay and saccadic activity with visually
guided than with memory-guided saccades, and both had broadly tuned
responses for disparity stimuli, suggesting that their visual receptive
fields have a three-dimensional configuration. These observations
indicate that the activity carried between parietal and frontal
cortical areas conveys a spectrum of signals but that the preponderance
of activity conveyed might be more closely related to earlier visual
processing than to the later saccadic stages that are directed to the SC.
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