Dynamic encoding of saccade sequences in primate frontal eye field †

Abstract Top-down attention, controlled by frontal cortical areas, is a key component of cognitive operations. How different neurotransmitters and neuromodulators flexibly change the cellular and network interactions with attention demands remains poorly understood. While acetylcholine and dopamine are critically involved, glutamatergic receptors have been proposed to play important roles. To understand their contribution to attentional signals, we investigated how ionotropic glutamatergic receptors in the frontal eye field (FEF) of male macaques contribute to neuronal excitability and attentional control signals in different cell types. Broad-spiking and narrow-spiking cells both required N-methyl-D-aspartic acid and α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor activation for normal excitability, thereby affecting ongoing or stimulus-driven activity. However, attentional control signals were not dependent on either glutamatergic receptor type in broad- or narrow-spiking cells. A further subdivision of cell types into different functional types using cluster-analysis based on spike waveforms and spiking characteristics did not change the conclusions. This can be explained by a model where local blockade of specific ionotropic receptors is compensated by cell embedding in large-scale networks. It sets the glutamatergic system apart from the cholinergic system in FEF and demonstrates that a reduction in excitability is not sufficient to induce a reduction in attentional control signals.

Download Full-text

Frontal eye field activity preceding aurally guided saccades

Journal of Neurophysiology ◽

10.1152/jn.1994.71.3.1250 ◽

1994 ◽

Vol 71 (3) ◽

pp. 1250-1253 ◽

Cited By ~ 84

Author(s):

G. S. Russo ◽

C. J. Bruce

Keyword(s):

Spatial Location ◽

Auditory Target ◽

Frontal Eye Field ◽

Visually Guided ◽

Movement Vector ◽

Initial Fixation ◽

Field Activity ◽

Eye Field ◽

Movement Field ◽

Visual Targets

1. We studied neuronal activity in the monkey's frontal eye field (FEF) in conjunction with saccades directed to auditory targets. 2. All FEF neurons with movement activity preceding saccades to visual targets also were active preceding saccades to auditory targets, even when such saccades were made in the dark. Movement cells generally had comparable bursts for aurally and visually guided saccades; visuomovement cells often had weaker bursts in conjunction with aurally guided saccades. 3. When these cells were tested from different initial fixation directions, movement fields associated with aurally guided saccades, like fields mapped with visual targets, were a function of saccade dimensions, and not the speaker's spatial location. Thus, even though sound location cues are chiefly craniotopic, the crucial factor for a FEF discharge before aurally guided saccades was the location of auditory target relative to the current direction of gaze. 4. Intracortical microstimulation at the sites of these cells evoked constant-vector saccades, and not goal-directed saccades. The direction and size of electrically elicited saccades generally matched the cell's movement field for aurally guided saccades. 5. Thus FEF activity appears to have a role in aurally guided as well as visually guided saccades. Moreover, visual and auditory target representations, although initially obtained in different coordinate systems, appear to converge to a common movement vector representation at the FEF stage of saccadic processing that is appropriate for transmittal to saccade-related burst neurons in the superior colliculus and pons.

Download Full-text

Acute activation and inactivation of macaque frontal eye field with GABA-related drugs

Journal of Neurophysiology ◽

10.1152/jn.1995.74.6.2744 ◽

1995 ◽

Vol 74 (6) ◽

pp. 2744-2748 ◽

Cited By ~ 81

Author(s):

E. C. Dias ◽

M. Kiesau ◽

M. A. Segraves

Keyword(s):

Injection Site ◽

Rhesus Monkeys ◽

Frontal Eye Field ◽

Surgical Removal ◽

Gamma Aminobutyric Acid ◽

Eye Field ◽

Distribution Of Points ◽

Direction Opposite ◽

Voluntary Saccades

1. This project tests the behavioral effects of reversible activation and inactivation of sites within the frontal eye field of rhesus monkeys with microinjections of the gamma-aminobutyric acid (GABA)-related drugs bicuculline and muscimol. 2. Muscimol injections impaired the monkeys' ability to make both visually and memory-guided saccades to targets at the center of the area represented by the injection site. The latencies of saccades to targets in regions flanking the injection were increased. For memory-guided saccades, saccades in the direction opposite to that represented by the injection site, were made with shorter latency than controls and often occurred before the movement cue. 3. Bicuculline injections produced irrepressible saccades equivalent to the saccade vector represented by the injection site, often in a staircase of several closely spaced movements. 4. Both substances decreased the accuracy of fixation of a central light. The distribution of points of fixation on different trials was diffuse, and the angle of gaze tended to deviate towards the side of the injection. 5. The results of these acute injections are similiar to those observed in the superior colliculus and are much more substantial than the effects observed in the long term after surgical removal of the frontal eye field. The results of this study promote a central role for the frontal eye field in the generation of all voluntary saccades and in the control of fixation.

Download Full-text

Disparity Sensitivity of Frontal Eye Field Neurons

Journal of Neurophysiology ◽

10.1152/jn.2000.83.1.625 ◽

2000 ◽

Vol 83 (1) ◽

pp. 625-629 ◽

Cited By ~ 55

Author(s):

Stefano Ferraina ◽

Martin Paré ◽

Robert H. Wurtz

Keyword(s):

Eye Movements ◽

Dimensional Space ◽

Visual Stimuli ◽

Three Dimensional ◽

Frontal Eye Field ◽

Visual Responses ◽

Motor Processes ◽

Uncrossed Disparity ◽

Eye Field ◽

Three Dimensional Space

Information about depth is necessary to generate saccades to visual stimuli located in three-dimensional space. To determine whether monkey frontal eye field (FEF) neurons play a role in the visuo-motor processes underlying this behavior, we studied their visual responses to stimuli at different disparities. Disparity sensitivity was tested from 3° of crossed disparity (near) to 3° degrees of uncrossed disparity (far). The responses of about two thirds of FEF visual and visuo-movement neurons were sensitive to disparity and showed a broad tuning in depth for near or far disparities. Early phasic and late tonic visual responses often displayed different disparity sensitivity. These findings provide evidence of depth-related signals in FEF and suggest a role for FEF in the control of disconjugate as well as conjugate eye movements.

Download Full-text

On the Evolution of the Frontal Eye Field: Comparisons of Monkeys, Apes, and Humans

Evolution of Nervous Systems ◽

10.1016/b978-0-12-804042-3.00130-5 ◽

2017 ◽

pp. 249-275 ◽

Cited By ~ 5

Author(s):

J.D. Schall ◽

W. Zinke ◽

J.D. Cosman ◽

M.S. Schall ◽

M. Paré ◽

...

Keyword(s):

Frontal Eye Field ◽

Eye Field

Download Full-text

Visually guided saccade versus eye-hand reach: contrasting neuronal activity in the cortical supplementary and frontal eye fields

Journal of Neurophysiology ◽

10.1152/jn.1996.75.5.2187 ◽

1996 ◽

Vol 75 (5) ◽

pp. 2187-2191 ◽

Cited By ~ 68

Author(s):

H. Mushiake ◽

N. Fujii ◽

J. Tanji

Keyword(s):

Eye Movement ◽

Neuronal Activity ◽

Motor Task ◽

Oculomotor Control ◽

Frontal Eye Field ◽

Frontal Eye Fields ◽

Saccadic Eye Movement ◽

Visually Guided ◽

Supplementary Eye Field ◽

Eye Field

1. We studied neuronal activity in the supplementary eye field (SEF) and frontal eye field (FEF) of a monkey during performance of a conditional motor task that required capturing of a target either with a saccadic eye movement (the saccade-only condition) or with an eye-hand reach (the saccade-and-reach condition), according to visual instructions. 2. Among 106 SEF neurons that showed presaccadic activity, more than one-half of them (54%) were active preferentially under the saccade-only condition (n = 12) or under the saccade-and-reach condition (n = 45), while the remaining 49 neurons were equally active in both conditions. 3. By contrast, most (97%) of the 109 neurons in the FEF exhibited approximately equal activity in relation to saccades under the two conditions. 4. The present results suggest the possibility that SEF neurons, at least in part, are involved in signaling whether the motor task is oculomotor or combined eye-arm movements, whereas FEF neurons are mostly related to oculomotor control.

Download Full-text