The proposed experiments continue an investigation of the functional organization of the primate frontal eye field (FEF) cortex and its role in the execution of voluntary eye movements. Previous studies of neurons in the saccadic region of FEF (FEFsac) find different combinations of activity related to saccades, visual inputs, and eye position as well as to behavioral states including memory and anticipation; similar activities related to smooth pursuit are found in FEF's smooth eye movement region (FEFsem). This new proposal initiates an investigation of how such activities and information are communicated between FEF and other areas that have strong reciprocal connections with FEF, demonstrated oculomotor function, and low thresholds for electrically eliciting eye movements. The parietal eye field (PEF) Iying in the lateral bank of the intraparietal sulcus (LIP) will be the principal structure studied. It is hypothesized that FEF receives visuospatial information coding possible saccadic targets from PEF, and that PEF receives activity coding impending saccadic eye movements from FEF. Communications between FEF and the oculomotor zone of the dorsal thalamus (termed thalamic eye field; TEF) will be the other pairing studied. It is hypothesized that FEF receives efferent copies of executing and completed saccadic eye movements from TEF, and that FEF efferents to TEF relay information about impending saccadic eye movements. For each of the pairings (PEF<->FEF and TEF<->FEF), 6 complementary experiments will be executed which Aim: 1) To determine what information/signals FEF sends to each target area by characterizing FEF neurons that are antidromically activated by electrodes in PEF and TEF. 2) To characterize information FEF receives from PEF and TEF by using the same methodology in reverse. 3) To analyze interareal communications by simultaneously recording from neurons with overlapping response fields in FEF and a target area, and analyzing possible causal relationships via cross-correlograms of their spiking during different behaviors. 4) To complement the cross-correlation analyses by directly stimulating the FEF neuron being recorded with very low-intensity pulses (1-10 pA) at low frequency (1-3 Hz) and examining post-stimulus histograms (PSTHs) of the PEF/TEF neuron for significant excitation. Direct activation of the FEF neuron by the PEF/TEF site will be examined via the same methodology in reverse. 5) To further test any causal relation indicated by Aims 3 or 4 by deactivating the presumed effector site with muscimol or lidocaine and reanalyzing the functional properties of the neuron at the presumed target site. 6) To provide fine anatomical details of these reciprocal connections via microinjections of BDA and other tracers at physiologically-characterized sites, both in FEF and in PEF or TEF. Thus, the overall objective of this proposal is to begin to characterize the coordination of the distributed network above the midbrain that directs voluntary eye movements. The ultimate objective is to unite such data within a model of FEF function that accurately relates to normal and abnormal sensorimotor behavior, and accounts for the predictive, mnemonic, and cognitive facets of FEF function.

National Institute of Health (NIH)
National Eye Institute (NEI)
Research Project (R01)
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Visual Sciences B Study Section (VISB)
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Hunter, Chyren
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Yale University
Schools of Medicine
New Haven
United States
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Stanton, Gregory B; Friedman, Harriet R; Dias, Elisa C et al. (2005) Cortical afferents to the smooth-pursuit region of the macaque monkey's frontal eye field. Exp Brain Res 165:179-92
Russo, G S; Bruce, C J (2000) Supplementary eye field: representation of saccades and relationship between neural response fields and elicited eye movements. J Neurophysiol 84:2605-21
Shi, D; Friedman, H R; Bruce, C J (1998) Deficits in smooth-pursuit eye movements after muscimol inactivation within the primate's frontal eye field. J Neurophysiol 80:458-64
Burman, D D; Bruce, C J (1997) Suppression of task-related saccades by electrical stimulation in the primate's frontal eye field. J Neurophysiol 77:2252-67
Russo, G S; Bruce, C J (1996) Neurons in the supplementary eye field of rhesus monkeys code visual targets and saccadic eye movements in an oculocentric coordinate system. J Neurophysiol 76:825-48
MacAvoy, M G; Bruce, C J (1995) Comparison of the smooth eye tracking disorder of schizophrenics with that of nonhuman primates with specific brain lesions. Int J Neurosci 80:117-51
Stanton, G B; Bruce, C J; Goldberg, M E (1995) Topography of projections to posterior cortical areas from the macaque frontal eye fields. J Comp Neurol 353:291-305
Dias, E C; Bruce, C J (1994) Physiological correlate of fixation disengagement in the primate's frontal eye field. J Neurophysiol 72:2532-7
Russo, G S; Bruce, C J (1994) Frontal eye field activity preceding aurally guided saccades. J Neurophysiol 71:1250-3
Gottlieb, J P; MacAvoy, M G; Bruce, C J (1994) Neural responses related to smooth-pursuit eye movements and their correspondence with electrically elicited smooth eye movements in the primate frontal eye field. J Neurophysiol 72:1634-53

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