JOURNALOFNEUROPHYSIOLOGY Vol. 58, No. 6, December 1987. Printed in U.S.A Functional Properties of Corticotectal Neurons in the Monkey’s Frontal Eye Field MARK A. SEGRAVES AND MICHAEL E. GOLDBERG Laboratory of SensorimotorResearch, National Eye Institute, National Institutes of Health, Bethesda,Maryland 20892 SUMMARY AND CONCLUSIONS 5. The remaining 20% of the corticotectal neurons were a heterogeneous group whose 1. We examined the activity of identified activity could not be classified as movement, corticotectal neurons in the frontal eye field visuomovement or foveal. Their responses of awake behaving rhesus monkeys (Macaca included postsaccadic, anticipatory, and re- mulatta). Corticotectal ne urons were anti- ward-related activity, as well as activity dromical y excited using biphasic cu rrent modulated during certain directions of pulses passedthrough monopolar microelec- smooth-pursuit eye movements. One neuron trodes within the superior colliculus. The ac- was unresponsive during all of the behavioral tivity of single corticotectal neurons was tasks used. There were no corticotectal studied while the m .onkey performed behav- neurons that could be classified as primarily ioral tasks designed to test the relation of the responsive to peripheral visual stimuli. neuron’s discharge to visual and oculomotor 6. Histological reconstructions of elec- events. trode penetrations localized corticotectal 2. Fifty-one frontal eye field corticotectal neurons to layer V of the frontal eye field. neurons were examined in two monkeys. For 22 corticotectal neurons tested, each had Current thresholds for antidromic excitation its minimum threshold for antidromic exci- ranged from 6 to 1,200 PA, with a mean of tation within the superior colliculus, as 330 PA. Antidromic latencies ranged from judged by either histological confirmation, 1.2 to 6.0 ms, with a mean of 2.25 ms. or surrounding neuronal responsesrecorded 3. Fifty-three percent of the identified through the stimulation microelectrode. The corticotectal neurons were classified as hav- majority of these neurons had minimum ing movement-related activity. They had lit- threshold sites within the intermediate tle or no response to visual stimuli, but very layers; a few minimum threshold sites were strong activity before both visually guided located within the superficial or deep collic- and memory-guided saccades.An additional ular layers. 6% of corticotectal n.eurons had v ,isuomove- 7. The lowest thresholds for antidromic ment activity, combining both a visual- and excitation were obtained when the optimal a saccade-related response. In each case, vi- saccade vectors associated with the frontal suomovement neurons antidromically ex- eye field recording and collicular stimulation cited from the superior colliculus had move- sites were closely matched. There was a ment-related activity, which was much strong correlation between a measure of the stronger than the visual component of their difference between saccadesassociated with response. recording and stimulation sites and the log of 4. Twenty-two percent of the corticotectal threshold for antidromic excitation. This re- neurons were primarily responsive to visual lationship was such that small increases in stimulation of the fovea. These included the vector difference between frontal eye both neurons responding to the onset and field and collicular saccadeswere accompa- neurons responding to the disappearance of a nied by large increases in threshold. light flashed on the fovea. 8. In comparison to the entire population 1387 1388 M. A. SEGRAVES AND M. E. GOLDBERG of frontal eye field neurons examined by field neurons were not related to spontane- Bruce and Goldberg (7), we conclude that ous saccades made in the dark. The only there is a selective enrichment within the neurons related to saccades were a small per- population of corticotectal projection centage (30/700) that became active only neurons for neurons with eye movement-re- after the initiation of a saccadic eye move- lated activity and neurons with fovea1 visual ment. More recent single-neuron studies activity, and a paucity of neurons with pe- have indicated a role for the frontal eye field ripheral visual receptive fields and postsac- in the initiation of saccades. Mohler, Gold- cadic activity. berg, and Wurtz (39) demonstrated that cells 9. These data suggest that the visual activ- in the frontal eye field discharge in response ity prevalent within the frontal eye field is to visual stimuli. This visual activity is en- likely to help generate the activity of move- hanced when the monkey makes a saccade to ment-related neurons, but it is not a source the stimulus in the receptive field (62), and for visual activity within the superior collic- the enhancement only occurs before sac- ulus. cades and not before arm movements or 10. The frontal eye field’s projection to other activity in which saccades do not occur the superior colliculus provides several mes- (9). Bruce and Goldberg (7) recently reported sages relevant for oculomotor performance, that only - 19% of frontal eye field neurons including information pertinent to the main- have purely postsaccadic activity. The ma- tenance and release of fixation, and targeting jority of neurons recorded from by Bruce information regarding an intended saccade. and Goldberg in awake behaving monkeys had some form of activity that preceded visually guided saccadic eye movements, INTRODUCTION including a range of neuron activity from Since Ferrier’s original demonstration ( 12) purely visual to purely movement related. that electrical stimulation of the monkey’s It is clear there are signals in the frontal eye prearcuate frontal cortex produced conju- field that could drive saccadic eye move- gate eye movements, it has been postulated ments and neural pathways by which these that this region participates in the voluntary signals could reach brain stem oculomotor control of gaze. However, a number of ex- centers. However, to understand how the ce- periments have raised questions about the rebral cortex controls a specific behavior, it is exact role of the frontal eye field in eye- not sufficient to know the types of activity in movement control. This uncertainty results, the cortex and the anatomical projections of in part, from the existence of parallel path- that region. One must also know what infor- ways that are likely to be involved in the mation is carried by the corticofugal signals. input of eye movement control signals to the These output signals are likely to be pro- brain stem ocuomotor centers. The frontal duced bv a subset of the activity types within eye field can affect the oculomotor system the entire neuronal population, and the out- via three pathways (26, 33-35, 55). The put population will be enriched for some sig- first is by a direct projection to perioculomo- nal types and lacking others. To begin to an- tor regions in the midbrain and pons (33). swer this question, we identified corticotectal The second is by a projection to the caudate projection neurons by antidromic excitation nucleus, which might then affect the inhibi- from the superior colliculus and then charac- tory pathway from the substantia nigra pars terized these neurons in awake behaving ani- reticulata to the superior colliculus (11, 24). mals according to the scheme described by The final one is a direct projection to the Bruce and Goldberg (7). A preliminary re- intermediate layers of the superior colliculus port of these experiments has been published (1, 30). The relative contribution that each elsewhere (5 3). pathway makes to eye-movement control has not been determined. Additional prob- METHODS lems arise when one considers the number of different neuron activity types that have Preoperative training been described in the frontal eye field. Bizzi Two adult rhesus monkeys (Macaca mulatta) (4) originally found that most frontal eye were trained preoperatively to do a simple visual FRONTAL EYE FIELD CORTICOTECTAL NEURONS fixation task using established techniques (60). criteria for eye position relative to target position The monkey was seated in a primate chair and and for saccade amplitude and direction, in order began a trial by pressing a metal bar in front of to receive a liquid reward. Eye position was mea- him. This resulted in the onset of a target light on sured by the magnetic search-coil system using the a screen in front of the monkey. The monkey was C.N.C. Engineering phase-sensitive detector. Eye required to detect the dimming of the light and position measurement was accurate to 15 min of signal this detection by releasing the metal bar to arc within a range of 20” from the center of gaze receive a liquid reward. and was not corrected for cosine error. Each monkey was trained to do several behav- Surgery ioral tasks (Fig. 1). Each task began with the ap- Surgery was performed under aseptic condi- pearance of a central stationary light on the screen tions. The monkey was anesthetized with ket- (Fig. 1, FP). The computer monitored the mon- amine hydrochloride (10 mg/kg im) followed by key’s eye position, and when the monkey had pentobarbital sodium through an intravenous achieved fixation for 100 ms the computer then catheter as needed. During the surgical procedure, began the various timing intervals of each task: a subconjunctival wire coil for the measurement 1) FIXATION TASK (FIG. 1A). The monkey was of eye position with the magnetic search-coil tech- required to hold fixation throughout the trial. nique was implanted in one eye (27,44). Trephine During some trials the fixation light was turned holes were made through the skull over the supe- off at an unpredictable moment for a brief period rior colliculi and over both left and right frontal of time. The interval during which the light was eye fields. Stainless steel bolts to strengthen the turned off was the same in any given block of bond of dental acrylic to the skull were fastened in trials, but was varied from 200 to 500 ms between slots cut through the skull and extending away blocks of trials.