Cristina Lucchetti

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.

Attention-related neurons in the supplementary eye field of the macaque monkey

This study investigated whether the neuronal activity of a cortical area involved in the control of eye fixation is affected by the covert orienting of attention. We recorded single-unit activity from the supplementary eye field (SEF) of two macaque monkeys performing fixation and peripheral-attention tasks. Ninety-nine out of four hundred and fifteen cells were related to eye movements. The other neurons showed relationship with postural adjustments, and arm and ear movements. Fifty-five neurons were active during fixation (fixation cells) and 44 discharged in relation to saccades. The experiments reported here primarily concern the fixation cells. The activity of 64% (35/55) of fixation cells started with the onset of visual stimulus, before the visual input reached the fovea, and continued during active fixation. The activity of 27% (15/55) of fixation cells started with the onset of fixation. The activity of 9% (5/55) of fixation cells modified their timing trial by trial. Sixty-four percent of the fixation cells (35/55) were position-dependent, showing a selective spatial field of activity, 36% (20/55) were position-independent and characterized by a full spatial field. None of the 55 cells showed a visual receptive field. We tested both types of fixation cells by means of a peripheral attention task. When attention was oriented peripherally toward a target located in the selective spatial field, the cells discharged as if the gaze was held toward it. When attention was oriented peripherally toward a target, lying outside the selective spatial field, the cells were inactive as if gaze was held in that position. These results suggest that the supplementary eye field neurons may code for oriented attention in space and might be involved in the preparation of motor action.

Behavioral and Motor Mechanisms of Dorsomedial Frontal Cortex of Macaca Monkey

The activity of 249 neurons in the dorsomedial frontal cortex was recorded in two macaca monkeys. The animals had been trained for saccades and fixation tasks in an unrestrained condition. We found 51 burst neurons that showed a double-firing discharge. We observed two different patterns of discharge. In one case the first burst occurred before the arm movement, the second before the related eye movement. In the second case, the first discharge took place before a neck contraction followed by a second burst before eye movement. Some cells showed two discharges, one that preceded the bar-press and the other the saccade. With other cells the discharges preceded the bar-release and then saccade. Still other cells discharged three times: first before the bar-press, second before release and third before the orienting saccade. Some cells were active for the bar-press and for the first orienting saccades. These cells were active also for a large range of movement tested at the presentation of natural stimuli. Electrical stimulation failed to evoke either arm or eye movement. Neck-eye cells are related to movement of the eye and to an increase of EMG activity independent of eye position. The electrical stimulation evoked eye movements and EMG increases at low threshold. The activity of arm-eye cells related to purposeful movement with the ineffectiveness of electrical stimulation may be ascribed to a motor reactivation or an ordering signal. The neck-eye cells may be considered trigger commands for neck-eye coordination.(ABSTRACT TRUNCATED AT 250 WORDS)

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.

Auditory environmental cells and visual fixation effect in area 8B of macaque monkey

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.

Auditory-motor and cognitive aspects in area 8B of macaque monkey's frontal cortex: a premotor ear-eye field (PEEF).

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).

Auditory and visual systems organization in Brodmann Area 8 for gaze-shift control: where we do not see, we can hear

Hearing is especially important for most primate species as they live in habitats of dense vegetation that limits vision. Stebbins (1980) summed up the evolution of the auditory system by assuming that earliest mammals exploited nocturnal niches since they were relatively free of many of the large, diurnal, predacious reptiles. Therefore, hearing and smell were more useful at night than vision. Our vision is limited not only in the dark but also outside the visual field. In fact, if we observe the behavior of a predator like a feline, oriented toward its prey, and at the same time a sound occurs behind, we might note three principal different behaviors: the predator could maintain its gaze and ears on the prey neglecting the sound source; the predator could maintain its gaze on the prey rotating ears and then shifting its auditory attention toward the sound source; finally the predator could break its attention and orient gaze and ears toward the sound source. A similar behavior is seen in human beings during social interaction with two or more interlocutors. In humans, orienting movements are carried out by the eyes, head, and/or body operating alone or in various combinations depending on the behavioral situation. However, in non-human primates, such as macaque monkeys, head orienting movements and, more generally, gaze-shift are accompanied by ear orienting movements, which allow the shifting of auditory attention toward a sound of interest (Bon and Lucchetti, 1994, 2006; Lucchetti et al., 2008; Lanzilotto et al., 2013; Yin, 2013). Considering all these assumptions, the auditory system could have an important role to detect information even from regions of the space that the visual system cannot explore without orienting movements. In other words, where we cannot see, we can hear. Through this opinion article, we argue that Brodmann Area 8 receives information from both auditory and visual systems and organizes a transformation of these sensory signals into gaze-shift motor commands. Our hypothesis is that this sensory-motor transformation is spatially organized, from both anatomical and functional points of view. Anatomical and functional properties of the Brodmann Area 8 (consisting in Area 8A plus Area 8B) support a medio-lateral organization for both auditory and visual systems. In particular, the lateral portion, corresponding to Area 8A or Frontal Eye Field (FEF), could play a role in receiving visual and auditory information from a central part of the visual field and then in organizing gaze-shift motor commands toward it. Otherwise, the medial portion, corresponding to Area 8B or Premotor Ear-Eye Field (PEEF), could play a role in receiving principally auditory information from a peripheral region of the space and then in organizing gaze-shift motor commands toward it.

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.