Motor intention activity in the macaque's lateral intraparietal area. I. Dissociation of motor plan from sensory memory

1996 ◽  
Vol 76 (3) ◽  
pp. 1439-1456 ◽  
Author(s):  
P. Mazzoni ◽  
R. M. Bracewell ◽  
S. Barash ◽  
R. A. Andersen

1. The lateral intraparietal area (area LIP) of the monkey's posterior parietal cortex (PPC) contains neurons that are active during saccadic eye movements. These neurons' activity includes visual and saccade-related components. These responses are spatially tuned and the location of a neuron's visual receptive field (RF) relative to the fovea generally overlaps its preferred saccade amplitude and direction (i.e., its motor field, MF). When a delay is imposed between the presentation of a visual stimulus and a saccade made to its location (memory saccade task), many LIP neurons maintain elevated activity during the delay (memory activity, M), which appears to encode the metrics of the next intended saccadic eye movements. Recent studies have alternatively suggested that LIP neurons encode the locations of visual stimuli regardless of where the animal intends to look. We examined whether the M activity of LIP neurons specifically encodes movement intention or the locations of recent visual stimuli, or a combination of both. In the accompanying study, we investigated whether the intended-movement activity reflects changes in motor plan. 2. We trained monkeys (Macaca mulatta) to memorize the locations of two visual stimuli and plan a sequence of two saccades, one to each remembered target, as we recorded the activity of single LIP neurons. Two targets were flashed briefly while the monkey maintained fixation; after a delay the fixation point was extinguished, and the monkey made two saccades in sequence to each target's remembered location, in the order in which the targets were presented. This "delayed double saccade" (DDS) paradigm allowed us to dissociate the location of visual stimulation from the direction of the planned saccade and thus distinguish neuronal activity related to the target's location from activity related to the saccade plan. By imposing a delay, we eliminated the confounding effect of any phasic responses coincident with the appearance of the stimulus and with the saccade. 3. We arranged the two visual stimuli so that in one set of conditions at least the first one was in the neuron's visual RF, and thus the first saccade was in the neuron's motor field (MF). M activity should be high in these conditions according to both the sensory memory and motor plan hypotheses. In another set of conditions, the second stimulus appeared in the RF but the first one was presented outside the RF, instructing the monkey to plan the first saccade away from the neuron's MF. If the M activity encodes the motor plan, it should be low in these conditions, reflecting the plan for the first saccade (away from the MF). If it is a sensory trace of the stimulus' location, it should be high, reflecting stimulation of the RF by the second target. 4. We tested 49 LIP neurons (in 3 hemispheres of 2 monkeys) with M activity on the DDS task. Of these, 38 (77%) had M activity related to the next intended saccade. They were active in the delay period, as expected, if the first saccade was in their preferred direction. They were less active or silent if the next saccade was not in their preferred direction, even when the second stimulus appeared in their RF. 5. The M activity of 8 (16%) of the remaining neurons specifically encoded the location of the most recent visual stimulus. Their firing rate during the delay reflected stimulation of the RF independently of the saccade being planned. The remaining 3 neurons had M activity that did not consistently encode either the next saccade or the stimulus' location. 6. We also recorded the activity of a subset of neurons (n = 38) in a condition in which no stimulus appeared in a neuron's RF, but the second saccade was in the neuron's MF. In this case the majority of neurons tested (23/38, 60%) became active in the period between the first and second saccade, even if neither stimulus had appeared in their RF. Moreover, this activity appeared only after the first saccade had started in all but two of

1996 ◽  
Vol 76 (5) ◽  
pp. 2907-2918 ◽  
Author(s):  
M. Schmidt

1. Neurons in the pretectal nuclear complex that project to the ipsilateral dorsal lateral geniculate nucleus (LGNd) were identified by antidromic activation after electrical LGNd stimulation in awake cats, and their response properties were characterized to retinal image shifts elicited either by external visual stimulus movements or during spontaneous saccadic eye movements on a stationary visual stimulus, and to saccades in darkness. Eye position was monitored with the use of a scleral search coil and care was taken to assure stability of the eyes during presentation of moving visual stimuli. 2. Of a total sample of 134 cells recorded, 27 neurons were antidromically activated by electrical LGNd stimulation. In addition, responses from neurons that were not activated from the LGNd were also analyzed, including 19 “retinal slip” cells, which selectively respond to slow horizontal stimulus movements, and 21 “jerk” cells, which are specifically activated by rapid stimulus shifts. All recorded neurons were located in the nucleus of the optic tract and in the posterior pretectal nucleus. 3. In the light, neurons identified as projecting to the LGNd responded maximally to saccadic eye movements and to externally generated sudden shifts of large visual stimuli. Slow stimulus drifts did not activate these neurons. Response latencies were shorter and peak activities were increased during saccades compared with pure visual stimulation. No systematic correlation between response latency, response duration, or the number of spikes in the response and saccade direction, saccade amplitude, or saccade duration was found. Saccades and rapid stimulus shifts in the light also activated jerk cells but not retinal slip cells. 4. All 27 antidromically activated neurons also responded to spontaneous saccadic eye movements in complete darkness. Responses to saccades in the dark, however, had longer response latencies and lower peak activities than responses to saccades in light. As in the light, response parameters in darkness seemed not to code specific saccade parameters. Cells that were not activated from LGNd were found to be unresponsive to saccades in the dark. 5. According to their specific activation by saccades in darkness, LGNd-projecting pretectal neurons are termed “saccade neurons” to distinguish them from other pretectal cell populations, in particular from jerk neurons, which show similar response properties in light. 6. The saccade-related activation of pretectal saccade neurons may be used to modulate visual responses of LGNd relay cells following saccadic eye movements. Because the pretectogeniculate projection in cat most likely is GABAergic and terminates on inhibitory LGNd interneurons, its activation may lead to a saccade-locked disinhibition of relay cells. This input could counter the strong inhibition induced in the LGNd after shifts of gaze direction and lead to a resetting of LGNd cell activity.


1988 ◽  
Vol 60 (3) ◽  
pp. 1036-1052 ◽  
Author(s):  
H. Noda ◽  
S. Murakami ◽  
J. Yamada ◽  
J. Tamada ◽  
Y. Tamaki ◽  
...  

1. Systematic exploration throughout the deep cerebellar nuclei and white matter disclosed that the region from which saccadic eye movements (saccades) were evoked with weak currents (less than 10 microA) was confined to the fastigial nucleus and the adjacent white matter. 2. When an electrode for stimulation was advanced in the cerebellum, saccades were evoked in the direction of the stimulated side (ipsilateral saccades) as it entered the low-threshold region. In some tracks, particularly when the electrode was advanced in the medial portion of the fastigial nucleus, the direction of the evoked saccades changed from the ipsilateral to the contralateral. 3. The mappings with microstimulation disclosed that the ipsilateral saccades were elicited from a relatively wide region that included almost the full extent of the fastigial nucleus. The low-threshold region continued in the white matter caudally into vermal lobule VII and rostrally into the dorsal aspect of the brachium conjunctivum. On the other hand, the contralateral saccades were evoked from a relatively circumscribed region in the ventromedial portion of the fastigial nucleus. 4. The reversal in the direction of the horizontal component occurred always in a narrow zone in the core of the fastigial nucleus. The caudal part of this zone coincided with an ellipsoidal region where anterogradely labeled axons of the Purkinje cells terminated when HRP was injected into vermal lobule VII. 5. When bicuculline (0.2-1 microgram) was injected in the ellipsoidal region, the ipsilateral saccades evoked from the dorsocaudal aspect of the region were suppressed for several hours. On the other hand, the contralateral saccades evoked from the ventromedial portion of the fastigial nucleus were either unchanged or enhanced. 6. Because the ipsilateral saccades were suppressed by bicuculline, they were most probably evoked by stimulation of the presynaptic component of gamma-amino-butyric acid-(GABA) mediated synapses, namely the axons of Purkinje cells. 7. Because stimulation of the presynaptic component of the inhibitory synapses evoked ipsilateral saccades, activation of the postsynaptic component would evoke contralateral saccades. In fact, the distribution of the fastigial sites yielding contralateral saccades coincided with the course of axons of fastigial neurons arising in the ellipsoidal region. It is most likely, therefore, that the contralateral saccades were evoked by stimulation of fastigial neurons.(ABSTRACT TRUNCATED AT 400 WORDS)


1988 ◽  
Vol 1 (1) ◽  
pp. 135-143 ◽  
Author(s):  
James T. McIlwain

AbstractEye movements were recorded with the scleral search coil method while striate cortex (area 17) was stimulated in alert cats with their heads fixed. Regardless of where stimulation was applied in the retinotopic map, eye position at the onset of stimulation strongly affected the amplitudes of evoked saccades, but had much less influence on their directions. Application of long stimulus trains evoked repeated saccades at all sites tested. Highly convergent or goal-directed saccades were not observed. Cortically evoked saccades appeared to habituate with repeated stimulation and had higher thresholds and longer latencies that those reported for saccades evoked from the superior colliculus. The directions of cortically evoked saccades generally agreed with those predicted from the retinotopic coordinates of the stimulus sites, but saccade amplitudes were usually lower than expected. It is suggested that these findings are consistent with certain characteristics of eye-head coordination in the cat's normal visual orienting behavior. The results are difficult to reconcile with the hypothesis that goal-directed saccades are a normal response to targets outside the cat's oculomotor range.


1996 ◽  
Vol 76 (3) ◽  
pp. 1457-1464 ◽  
Author(s):  
R. M. Bracewell ◽  
P. Mazzoni ◽  
S. Barash ◽  
R. A. Andersen

1. In the companion paper we reported that the predominant signal of the population of neurons in the lateral intraparietal area (area LIP) of the monkey's posterior parietal cortex (PPC) encode the next intended saccadic eye movement during the delay period of a memory-saccade task. This result predicts that, should be monkey change his intention of what the next saccade will be, LIP activity should change accordingly to reflect the new plan. We tested this prediction by training monkeys to change their saccadic plan on command and recording the activity of LIP neurons across plan changes. 2. We trained rhesus monkeys (Macaca mulatta) to maintain fixation on a light spot as long as this spot remained on. During this period we briefly presented one, two, or three peripheral visual stimuli in sequence, each followed by a delay (memory period, M). After the final delay the fixation spot was extinguished, and the monkey had to quickly make a saccade to the location of the last target to have appeared. The monkey could not predict which stimuli, nor how many, would appear on each trial. He thus had to plan a saccade to each stimulus as it appeared and change his saccade plan whenever a stimulus appeared at a different location. 3. We recorded the M period activity of 81 area LIP neurons (from 3 hemispheres of 2 monkeys) in this task. We predicted that, if a neuron's activity reflected the monkey's planned saccade, its activity should be high while the monkey planned a saccade in the neuron's motor field (MF), and low while the planned saccade was in the opposite direction. The activity of most of the neurons in our sample changed in accordance with our hypothesis as the monkey's planned saccade changed. 4. In one condition the monkey was instructed by visual stimuli to change his plan from a saccade in the neuron's preferred direction to a saccade planned in the opposite direction. In this condition activity decreased significantly (P < 0.05) in 65 (80%) of 81 neurons tested. These neurons' activity changed to reflect the new saccade plan even though the cue for this change was not presented in their RF. 5. As a control we randomly interleaved, among trials requiring a plan change, trials in which the monkey had to formulate two consecutive plans to make a saccade in the neuron's preferred direction. The activity remained unchanged (P < 0.05) in 22 of 31 neurons tested (79%), indicating that the neurons continued to encode the same saccade plan. 6. In a variant of the task, the cue to the location of the required saccade was either a light spot or a noise burst from a loudspeaker. Of 22 neurons tested in this task, 16 (73%) showed activity changes consistent with plan changes cued by visual or auditory stimuli. 7. Alterations in the monkey's intentions, even in the absence of overt behavior, are manifested in altered LIP activity. These activity changes could be induced whether visual or auditory cues were used to indicate the required plan changes. Most LIP neurons thus do not encode only the locations of visual stimuli, but also the intention to direct gaze to specific locations, independently of whether a gaze shift actually occurs.


Brain ◽  
1993 ◽  
Vol 116 (2) ◽  
pp. 355-367 ◽  
Author(s):  
A. Priori ◽  
L. Bertolasi ◽  
J. C. Rothwell ◽  
B. L. Day ◽  
C. D. Marsden

2018 ◽  
Vol 119 (6) ◽  
pp. 2082-2090
Author(s):  
Yoshiko Izawa ◽  
Hisao Suzuki

Focal stimulation in the frontal eye field (FEF) evoked eye movements that were often accompanied by neck movements. Experiments were performed with concurrent recording of both movements in trained monkeys. We recorded neck forces under a head-restrained condition with a force-measuring system. With the system, we measured forces along the x-, y-, and z-axes and torque about the z-axis. Torque about the z-axis that represented yaw rotation of the head was significantly affected by stimulation. We found that stimulation generated two types of motor actions of the eyes and neck. In the first type, contraversive neck forces were evoked by stimulation of the medial part of the FEF, where contraversive saccadic eye movements with large amplitudes were evoked. When the stimulus intensity was increased, saccades were evoked in an all-or-none manner, whereas the amplitude of neck forces increased gradually. In the second type, contraversive neck forces were evoked by stimulation of the medial and caudal part of the FEF, where ipsiversive slow eye movements were evoked. The depth profiles of amplitudes of neck forces were almost parallel to those of eye movements in individual stimulation tracks. The present results suggest that the FEF is involved in the control of motor actions of the neck as well as the eyes. The FEF area associated with contraversive saccades and contraversive neck movements may contribute to a gaze shift process, whereas that associated with ipsiversive slow eye movements and contraversive neck movements may contribute to a visual stabilization process. NEW & NOTEWORTHY Focal stimulation in the frontal eye field (FEF) evoked eye and neck movements. We recorded neck forces under a head-restrained condition with a force-measuring system. Taking advantage of this approach, we could analyze slow eye movements that were dissociated from the vestibuloocular reflex. We found ipsiversive slow eye movements in combination with contraversive neck forces, suggesting that the FEF may be a source of a corollary discharge signal for compensatory eye movements during voluntary neck movements.


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