The activity of 249 neurons in the dorsomedial frontal cortex was studied in two macaque monkeys. The animals were trained to release a bar when a visual stimulus changed color in order to receive reward. An acoustic cue signaled the start of a series of trials to the animal, which was then free to begin each trial at will. The monkeys tended to fixate the visual stimuli and to make saccades when the stimuli moved. The monkeys were neither rewarded for making proper eye movements nor punished for making extraneous ones. We found neurons whose discharge was related to various movements including those of the eye, neck, and arm. In this report, we describe the properties of neurons that showed activity related to visual fixation and saccadic eye movement. Fixation neurons discharged during active fixation with the eye in a given position in the orbit, but did not discharge when the eye occupied the same orbital positions during nonactive fixation. These neurons showed neither a classic nor a complex visual receptive field, nor a foveal receptive visual field. Electrical stimulation at the site of the fixation neurons often drove the eye to the orbital position associated with maximal activity of the cell. Several different kinds of neurons were found to discharge before saccades: 1) checking-saccade neurons, which discharged when the monkeys made self-generated saccades to extinguish LED's; 2) novelty-detection saccade neurons, which discharged before the first saccade made to a new visual target but whose activity waned with successive presentations of the same target. These results suggest that the dorsomedial frontal cortex is involved in attentive fixation. We hypothesize that the fixation neurons may be involved in codifying the saccade toward a target. We propose that their involvement in arm-eye-head motor-planning rests primarily in targeting the goal of the movement. The fact that saccade-related neurons discharge when the saccades are self initiated, implies that this area of the cortex may share the control of voluntary saccades with the frontal eye fields and that the activation is involved in intentional motor processes.
In previous reports, we showed the involvement of area 8B neurons in both spontaneous ear and eye movement and in auditory information processing. Audition-related cells responded to complex environmental stimuli, but not to pure tones, and their activity changed during visual fixation as a possible inhibitory expression of the engagement of attention. We observed auditory, auditory-motor and motor cells for both eye and ear movements. This finding suggests that area 8B may be involved in the integration of auditory input with ear and eye motor output. In this paper, we extended these previous studies by examining area 8B activity in relation to auditive orienting behaviour, as well as the ocular orientation (i.e., visual fixation) studied previously. Visual fixation led to inhibition of activity in auditory and auditory-motor cells, which suggests that attention may be involved in both, maintaining the eye position and reducing the response of these cell types. Accordingly, during a given task or natural behaviour, spatial attention seems to affect more than one sensorimotor channel simultaneously. These data add to our understanding of how the neural network, through a two-channel attentive process, accomplishes to switch between two effectors, namely eyes and ears. Considering the functional, anatomical and cytoarchitectonic differences among the frontal eye field (FEF), the supplementary eye field (SEF) and area 8B, we propose to consider area 8B as a separate premotor ear-eye field (PEEF).
We evoked both ear and eye movements in area 8b, the rostral area of frontal cortex, in two monkeys. In some sites it was possible to evoke only ear movements or only eye movements; in other locations we evoked both ear and eye movements by varying the intensity of electrical stimulation. The electrically evoked ear movements were forward, or backward, or oblique (upward-forward; upward-backward). In two penetrations the ear movements were bilateral, in the other penetrations they were contralateral. Ipsilateral ear movements were not observed. The evoked eye movements were mainly fixed-vector saccades, contralateral and with an upward orientation of about 45 degrees. If we considered only the sites where the threshold was equal to or lower than 50 microA, the stimulation of this area evoked mainly ear movements. In addition we recorded the electrical activity of 195 neurons. Of these neurons: 74% (145/195) discharged before ear movements (ear cells); 20% (40/195) discharged before ear and eye movements (ear-eye cells); 5% (10/195) discharged only before eye movements (eye cells). Ninety-one percent (132/145) of ear cells presented a preferred direction; 90% (36/40) of ear-eye cells presented a preferred direction for ear movements, and 15% (6/40) presented a preferred direction for eye movements. Eighty-five percent (34/40) of cells did not present a preferred direction for visually guided saccades and were active when the monkey made saccades toward the unlit targets (checking saccades). Our results show that a field of area 8b is related to ear movements and to eye-ear movements. The findings that it is possible to obtain both ear and eye movements with low-intensity currents and that there are cells firing for the two types of movements suggest that area 8b may be involved in the orientation and coordination of both ear and eye. This area might be considered a rostral extension of supplementary eye field (SEF) or a different region. However, based on its distinct functional characteristics and connectivity, it is probably better regarded as a separate field. Regardless, the combination of 8b and SEF may constitute a cortical center for orienting processes.
A voluntary motor act, executed in response to a stimulus, requires both spatial and temporal computation. Even though electrophysiological and positron emission tomography (PET) investigations on humans suggest that SMA, medial prefrontal cortex and primary motor cortex play a role in temporal mechanisms, we have few data about neuronal time computation in the premotor cortex. The involvement of monkey premotor area (PM) in motor learning and cognitive processes, and the presence of buildup neurons, whose activity is closely related to the motor action, prompted us to investigate the involvement of these set-related neurons in the time domain. To this end we manipulated the duration of a pre-cue in a visuomotor task while recording unit activity. We found that, when the duration of the pre-cue was predictable and long (5 s), delay of the onset of cell activity in consecutive trials gradually increased. On the other hand, when the duration was unpredictable or predictable and short (1 s), this phenomenon could not be detected. The inconsistent discharge correlations with expected reward and attentional processes, and the specific discharge relationship to the time instruction, suggest that these buildup neurons reflect a learning process in the time domain.
Area 8B may be treated as part of either the prefrontal cortex or the premotor cortex. Previous investigations showed an involvement of area 8B in both eye and ear motor control and in auditory perception. In this report, we studied 139 neurons in three macaque monkeys of these, 32 neurons showed an activity related to environmental auditory stimuli. Fifteen cells with auditory characteristics (15/32) presented a firing discharge inhibited during the execution of visual fixation. The remaining 107 units presented complex or indefinable behaviour. The presence of auditory environmental cells which activity is related prevalently to the voice of persons (researchers) suggests that area 8B may be an area involved in auditory cross-modal association, in natural behaviour. The inhibitory effects during visual fixation suggest that area 8B is part of the inhibitory network preventing the gaze shift in relation to an auditory stimulus. This may be the consequence of the engagement of attention during fixation that may affect the auditory perception. Both aspects indicate that area 8B is involved in high cognitive processes in auditory and orienting processes.
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