L. Bon

The dorsomedial frontal cortex of the macaca monkey: fixation and saccade-related activity

SummaryThe 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 LEDs; 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 saccaderelated 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.

Ear and eye representation in the frontal cortex, area 8b, of the macaque monkey: an electrophysiological study.

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°. If we considered only the sites where the threshold was equal to or lower than 50 μA, 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.

Neuronal activity correlated with eye movement in the cat's pretectum

Single unit activity correlated with horizontal and vertical saccades was recorded in darkness from n. pretectalis anterior (NPA), n. pretectalis olivaris (NPO), n. tractus opticus (NTO) and n. pretectalis posterior (NPP). The units studied fell into two classes. The first class neurons displayed a high frequency burst of activity prior to the onset of a saccade regardless of where the eye was when the movement started. These neuronal reponses, mainly recorded from NPA and NPO, can therefore be ascribed to the motor aspect of the eye movement. The second type units, mostly found in NPP and NTO, responded after the initiation of a saccade and might be ascribed to a postsaccadic facilitation related to the visual attention during the fixation period.

Neurons signalling the maintenance of attentive fixation in frontal area 6aβ of macaque monkey

SummaryTwelve out of 140 neurons recorded in a restricted region of the frontal agranular cortex (area 6aβ) of trained macaque monkeys, discharged only during attentive fixation of a target in the straight ahead position. These cells, lacking a visual receptive field, were silent when the animals eye was in the same position during spontaneous oculomotor behaviour. Our preliminary results suggest that this area is involved in the codification of attentive fixation.

Neglect syndrome for aversive stimuli in a macaque monkey with dorsomedial frontal cortex lesion

After a session of unit activity recording, one of our monkeys presented an epileptic attack, which provoked contralateral tilting movements. The following days, the animal performed saccades and fixation tasks correctly in all directions, while contralateral arm reaching movements were severely impaired. To establish if the neurological lesion had changed the orienting performance we considered two types of stimuli, pleasant and aversive. Pleasant stimuli, presented in the ipsilateral or contralateral hemifield, readily drew the attention of the animal. If the same stimuli were presented simultaneously in both hemifields, the monkey oriented itself only toward the ipsilateral one. Aversive stimuli evoked an aggressive reaction only when the stimulus was localized in the ipsilateral hemifield. The animal clearly neglected the aversive stimulus presented in the contralateral hemifield. The animal recovered completely in 30 days. The postmortem examination revealed a lesion in the dorsomedial frontal cortex. The combined attentional and motor deficits suggest that this area may be involved in the preparation and execution of movements triggered by the affective meaning of the stimulus.

The motor programs of monkey's saccades: an attentional hypothesis

SummaryWe analyzed the dynamics of saccadic eye movements performed by monkeys in three different conditions: as a part of an ocular motor task, spontaneously when the monkey was alert but not performing a task in ordinary room illumination, and spontaneously when the monkey was alert but not performing a task in total darkness. We found three general classes of saccades: 1) regular-symmetric, in which the rise time of the velocity profile was equal to the falling time; 2) regular-asymmetric, in which the rise time was less than the falling time; 3) irregular, in which there were multiple velocity maxima or inflection points. The monkeys made irregular saccades half the time in the two spontaneous saccade conditions, and almost never during the task. In order to see if the regularity of saccades was an artifact of reward, we then evoked saccades by presenting the monkeys with novel visual and acoustic stimuli to which they made saccades. Such guided saccades to novel stimuli had regular velocity profiles. We suggest that saccades made as a part of attentive behavior differ in their motor programming from saccades made spontaneously in darkness, or saccades made in the light without a purpose relevant to visual behavior.

Oculomotor Corollary Discharge in the Cat Pretectum

Unit activity bursting after the onset of spontaneous eye movements made in total darkness has been recorded from the nucleus of the optic tract (NOT) of the cat pretectum. The present experiments are aimed at determining the functional significance of these neuronal reactions, namely whether the NOT discharge results from an afferent input arising from eye muscle proprioceptors or from a central signal (corollary discharge or efference copy). The results point to a central, rather than a peripheral, origin for NOT discharge. After both eyes have been paralysed, and therefore after eye-muscle proprioceptive input has been removed, NOT activity remained time-locked with increased activity in motoneurons of the III nerve nucleus.

Does attention affect the motor programs of pharmacologically induced eye movements

Attention plays an important role in oculomotor function. We studied the effect of attentional stimuli on eye movements induced by ketamine. The experiments were carried out on three monkeys. Ketamine injected intramuscularly induced nystagmus. When we switched on a new stimulus these eye movements stopped and the animal made a saccade toward it. This may be due to a new motor program, triggered by a visual stimulus, that among its characteristics is able to engage the animals attention. The program of evoked saccade is overwritten on induced oculomotor activity. Our results suggest that attentional processes modify the dynamic characteristics and induce in particular behavioral condition a new motor program.

Analogue analyser for on-line eye movement detection

A system of single movement detection is obtained by discriminating the velocities and orientations of eye ball displacements. The orthogonal components of eye velocity (Vx and Vy) are generated from the horizontal (X) and the vertical (Y) components of the movements by means of two derivative circuits and the velocity modulus (V) is generated through a vector operator from Vx and Vy. The onset and end of individual movements are detected on the basis of a preselected V, Vx or Vy threshold and, for every movement thus identified, the integral function of V(t), Vx(t) or Vy(t), characteristic of the type of movement, is generated in such a way that its final value represents ball displacement.

The spontaneous eye movements in the awake kitten.

The spontaneous eye movements were analysed comparatively in the kitten and in the cat. The eye movements were recorded in the dark by a magnetic search coil technique. The spatio-temporal organization of eye movements in the kitten has a prevailing vertical orientation and differs completely from that of the cat. In the kitten the amplitude of eye movements is smaller than in the cat and only a few movements are followed by fixation. It results, by correlating amplitude-peak velocity, that rapid eye movements in the awake kitten are saccades. From our results we conclude that the eye movements in the kitten and in the cat differ in many aspects and that the visual system is responsible for the development of the correct oculomotor behaviour.