Changing directions of forthcoming arm movements: neuronal activity in the presupplementary and supplementary motor area of monkey cerebral cortex

1. To understand roles played by two cortical motor areas, the presupplementary motor area (pre-SMA) and supplementary motor area (SMA), in changing planned movements voluntarily, cellular activity was examined in two monkeys (Macaca fuscata) trained to perform an arm-reaching task in which they were asked to press one of two target buttons (right or left) in three different task modes. 2. In the first mode (visual), monkeys were visually instructed to result and press either a right or left key in response to a forth coming trigger signal. In the second mode (stay), monkeys were required to wait for the trigger signal and press the same target key as pressed in preceding trials. In the third mode (shift), a 50 Hz auditory cue instructed the monkey to shift the target of the future reach from the previous target to the previous nontarget. 3. While the monkeys were performing this task, we recorded 399 task-related cellular activities from the SMA and the pre-SMA. Among them, we found a group of neurons that exhibited activity changes related specifically to shift trials (shift-related cells). The following properties characterized these 112 neurons. First, they exhibited activity changes after the onset of the 50-Hz auditory cue and before the movement execution when the monkeys were required to change the direction of forthcoming movement. Second, they were not active when the monkeys pressed the same key without changing the direction of the movements. Third, they were not active when the monkeys received the 50-Hz auditory cue but failed to change the direction of the movements by mistake. These observations indicate that the activity of shift-related cells is related to the redirection of the forthcoming movements, but not to the auditory instruction itself or to the location of the target key or the direction of the forthcoming movements. 4. Although infrequently, monkeys made errors in the stay trials and changed directions of the reach voluntarily. In that case, a considerably high proportion of shift-related neurons (12 of 19) exhibited significant activity changes long before initiation of the reach movement. These long-lasting activities were not observed during the preparatory period in correct stay trials, but resembled the shift-related activity observed when the target shift was made toward the same direction. Thus these activity changes were considered to be also related to the process of changing the intended movements voluntarily. 5. We found another population of neurons that showed activity modulation when the target shift was induced by the visual instruction in visual trials (visually guided shift-related neurons). These neurons were active when the light-emitting diode (LED) guided the forthcoming reach to the previous nontarget but not to the previous target. Therefore their activity was not a simple visual response to the LED per se. A majority of them also showed shift-related activity in shift trials (19 of 22 in monkey 2). 6. Neurons exhibiting the shift-related activity were distributed differentially among the two areas. In the pre-SMA, 31% of the neurons recorded showed the shift-related activity, whereas in the SMA, only 7% showed such an activity. These results suggest that pre-SMA and SMA play differential roles in updating the motor plans in accordance with current requirements.     

Apparent decrease in population clearance of theophylline: implications for dosage

Tthe antisaccade eye movement task, which has been linked to frontal lobe function, presents a target in one visual field and asks subjects to move their eyes to the same location in the opposite field. The task requires inhibition of the reflexive prosaccade to the cue, initiation of the antisaccade to the opposite field, and visuo-spatial memory of the cue location. Forty-two subjects from 19-79 years of age performed this task and a control task, visually guided saccades to the cue itself, to determine which functions are affected by aging. The time to initiate antisaccades increased linearly with age at a rate greater than the time to initiate visually guided saccades. This difference suggests that the processing time to inhibit the incorrect movement to the cue is selectively increased with age. Older subjects also made more incorrect prosaccadic movements to the cue, a finding consistent with the loss of inhibitory processing capacity. The accuracy of movements did not change, which suggests that visuo-spatial memory is unaffected by aging.     

Superior colliculus and active navigation: role of visual and non-visual cues in controlling cellular representations of space

To begin investigation of the contribution of the superior colliculus to unrestrained navigation, the nature of behavioral representation by individual neurons was identified as rats performed a spatial memory task. Similar to what has been observed for hippocampus, many superior collicular cells showed elevated firing as animals traversed particular locations on the maze, and also during directional movement. However, when compared to hippocampal place fields, superior collicular location fields were found to be more broad and did not exhibit mnemonic properties. Organism-centered spatial coding was illustrated by other neurons that discharged preferentially during right or left turns made by the animal on the maze, or after lateralized sensory presentation of somatosensory, visual, or auditory stimuli. Nonspatial movement-related neurons increased or decreased firing when animals engaged in specific behaviors on the maze regardless of location or direction of movement. Manipulations of the visual environment showed that many, but not all, spatial cells were dependent on visual information. The majority of movement-related cells, however, did not require visual information to establish or maintain the correlates. Several superior collicular cells fired in response to multiple maze behaviors; in some of these cases a dissociation of visual sensitivity to one component of the behavioral correlate, but not the other, could be achieved for a single cell. This suggests that multiple modalities influence the activity of single neurons in superior colliculus of behaving rats. Similarly, several sensory-related cells showed dramatic increases in firing rate during the presentation of multisensory stimuli compared to the unimodal stimuli. These data reveal for the first time how previous findings of sensory/motor representation by the superior colliculus of restrained/anesthetized animals might be manifested in freely behaving rats performing a navigational task. Furthermore, the findings of both visually dependent and visually independent spatial coding suggest that superior colliculus may be involved in sending visual information for establishing spatial representations in efferent structures and for directing spatially-guided movements.     

Response properties of saccade-related burst neurons in the central mesencephalic reticular formation

We studied the activity of saccade-related burst neurons in the central mesencephalic reticular formation (cMRF) in awake behaving monkeys. In experiment 1, we examined the activity of single neurons while monkeys performed an average of 225 delayed saccade trials that evoked gaze shifts having horizontal and vertical amplitudes between 2 and 20 degrees . All neurons studied generated high-frequency bursts of activity during some of these saccades. For each neuron, the duration and frequency of these bursts of activity reached maximal values when the monkey made movements within a restricted range of horizontal and vertical amplitudes. The onset of the movement followed the onset of the burst by the longest intervals for movements within a restricted range of horizontal and vertical amplitudes. The range of movements for which this interval was longest varied from neuron to neuron. Across the population, these ranges included nearly all contraversive saccades with horizontal and vertical amplitudes between 2 and 20 degrees. In experiment 2, we used the following task to examine the low-frequency prelude of activity that cMRF neurons generate before bursting: the monkey was required to fixate a light-emitting diode (LED) while two eccentric visual stimuli were presented. After a delay, the color of the fixation LED was changed, identifying one of the two eccentric stimuli as the saccadic target. After a final unpredictable delay, the fixation LED was extinguished and the monkey was reinforced for redirecting gaze to the identified saccadic target. Some cMRF neurons fired at a low frequency during the interval after the fixation LED changed color but before it was extinguished. For many neurons, the firing rate during this interval was related to the metrics of the movement the monkey made at the end of the trial and, to a lesser degree, to the location of the eccentric stimulus to which a movement was not directed.     

Increased dependence on visual information for movement control in patients with Parkinson's disease

Studies were made of visually and non-visually guided movements by patients with Parkinson's disease. The subjects moved a light, horizontal handle using rotation primarily about the elbow. During visually guided trials both handle and target positions were displayed to the subject; during non-visually guided trials only the handle position was displayed. During non-visually guided trials all patients showed a tendency for an overall flexion drift, although there was no change in average movement amplitude. The overall error in position by the end of the non-visually guided trials was greatly in excess of the reported values for passive displacement thresholds in normal subjects. It is suggested that the data indicate an increased dependence on visual information for control of motor activity in Parkinson's patients.     

Eye position effects on the neuronal activity of dorsal premotor cortex in the macaque monkey

Visual inputs to the brain are mapped in a retinocentric reference frame, but the motor system plans movements in a body-centered frame. This basic observation implies that the brain must transform target coordinates from one reference frame to another. Physiological studies revealed that the posterior parietal cortex may contribute a large part of such a transformation, but the question remains as to whether the premotor areas receive visual information, from the parietal cortex, readily coded in body-centered coordinates. To answer this question, we studied dorsal premotor cortex (PMd) neurons in two monkeys while they performed a conditional visuomotor task and maintained fixation at different gaze angles. Visual stimuli were presented on a video monitor, and the monkeys made limb movements on a panel of three touch pads located at the bottom of the monitor. A trial begins when the monkey puts its hand on the central pad. Then, later in the trial, a colored cue instructed a limb movement to the left touch pad if red or to the right one if green. The cues lasted for a variable delay, the instructed delay period, and their offset served as the go signal. The fixation spot was presented at the center of the screen or at one of four peripheral locations. Because the monkey's head was restrained, peripheral fixations caused a deviation of the eyes within the orbit, but for each fixation angle, the instructional cue was presented at nine locations with constant retinocentric coordinates. After the presentation of the instructional cue, 133 PMd cells displayed a phasic discharge (signal-related activity), 157 were tonically active during the instructed delay period (set-related or preparatory activity), and 104 were active after the go signal in relation to movement (movement-related activity). A large proportion of cells showed variations of the discharge rate in relation to limb movement direction, but only modest proportions were sensitive to the cue's location (signal, 43%; set, 34%; movement, 29%). More importantly, the activity of most neurons (signal, 74%; set, 79%; movement, 79%) varied significantly (analysis of variance, P < 0.05) with orbital eye position. A regression analysis showed that the neuronal activity varied linearly with eye position along the horizontal and vertical axes and can be approximated by a two-dimensional regression plane. These data provide evidence that eye position signals modulate the neuronal activity beyond sensory areas, including those involved in visually guided reaching limb movements. Further, they show that neuronal activity related to movement preparation and execution combines at least two directional parameters: arm movement direction and gaze direction in space. It is suggested that a substantial population of PMd cells codes limb movement direction in a head-centered reference frame.     

Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements

Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. J. Neurophysiol. 80: 3247-3260, 1998. To study the involvement of the supplementary (SMA) and presupplementary (pre-SMA) motor areas in performing sequential multiple movements that are individually separated in time, we injected muscimol, a gamma-aminobutyric acid agonist, bilaterally into the part of each area that represents the forelimb. Two monkeys were trained to perform three different movements, separated by a waiting time, in four or six different orders. First, each series of movements was learned during five trials guided by visual signals that indicated the correct movements. The monkeys subsequently executed the three movements in the memorized order, without the visual signals. After the injection of muscimol (3 microliter, 5 micrograms/microliters in 10 min) into either the SMA or pre-SMA bilaterally, the animals started making errors in performing the sequence of movements correctly from memory. However, when guided with a visual signal, they could select and perform the three movements correctly. The impaired memory-based sequencing of movements worsened progressively with time until the animals could not perform the task. Yet they still could associate the visual signals with the different movements at that stage. In control experiments on two separate monkeys, we found that injections of the same amount of muscimol into either the SMA or pre-SMA did not cause problems with nonsequential reaching movement regardless of whether it was visually triggered or self-initiated. These results support the view that both the SMA and pre-SMA are crucially involved in sequencing multiple movements over time.     

Sustained activity in the medial wall during working memory delays

We have taken advantage of the temporal resolution afforded by functional magnetic resonance imaging (fMRI) to investigate the role played by medial wall areas in humans during working memory tasks. We demarcated the medial motor areas activated during simple manual movement, namely the supplementary motor area (SMA) and the cingulate motor area (CMA), and those activated during visually guided saccadic eye movements, namely the supplementary eye field (SEF). We determined the location of sustained activity over working memory delays in the medial wall in relation to these functional landmarks during both spatial and face working memory tasks. We identified two distinct areas, namely the pre-SMA and the caudal part of the anterior cingulate cortex (caudal-AC), that showed similar sustained activity during both spatial and face working memory delays. These areas were distinct from and anterior to the SMA, CMA, and SEF. Both the pre-SMA and caudal-AC activation were identified by a contrast between sustained activity during working memory delays as compared with sustained activity during control delays in which subjects were waiting for a cue to make a simple manual motor response. Thus, the present findings suggest that sustained activity during working memory delays in both the pre-SMA and caudal-AC does not reflect simple motor preparation but rather a state of preparedness for selecting a motor response based on the information held on-line.     

Bilateral interactions in saccade programming. A saccade-latency study

Subjects were required to make a saccade to a target appearing randomly 4 degree to the left or right of the current fixation position (1280 trials per experiment). Location cues were used to direct visual attention and start saccade preparation to one of the two locations before target onset. When the cue indicated the target location (valid trials), the generation of express saccades (visually guided saccades with latencies around 100 ms) was strongly facilitated. When the opposite location was cued (invalid trials), express saccades were abolished and replaced by a population of mainly fast-regular saccades (latencies around 150 ms). This was found with a peripheral cue independently of whether the fixation point was removed before target onset (gap condition; experiment 1) or remained on throughout the trial (overlap condition; experiment 2). The same pattern also was observed with a central cue that did not involve any visual stimulation at a peripheral location (experiment 3). In the case where the primary saccade was executed in response to the cue and the target appeared at the opposite location, continuous amplitude transition functions were observed: starting at about 60-70 ms from target onset onward, the amplitude of the cue-elicited saccades continuously decreased from 4 degree to values below 1 degree. The results are explained by a fixation-gating model, according to which the antagonism between fixation and saccade activity gives rise to multimodal distributions of saccade latencies. It is argued that allocation of visual attention and saccade preparation to one location entails a successive disengagement of the fixation system controlling saccade preparation within the hemifield to which the saccade is prepared and a partial engagement of the opposite fixation system.     

Effects of saccades on the activity of neurons in the cat lateral geniculate nucleus

Effects of saccades on individual neurons in the cat lateral geniculate nucleus (LGN) were examined under two conditions: during spontaneous saccades in the dark and during stimulation by large, uniform flashes delivered at various times during and after rewarded saccades made to small visual targets. In the dark condition, a suppression of activity began 200-300 ms before saccade start, peaked approximately 100 ms before saccade start, and smoothly reversed to a facilitation of activity by saccade end. The facilitation peaked 70-130 ms after saccade end and decayed during the next several hundred milliseconds. The latency of the facilitation was related inversely to saccade velocity, reaching a minimum for saccades with peak velocity >70-80 degrees /s. Effects of saccades on visually evoked activity were remarkably similar: a facilitation began at saccade end and peaked 50-100 ms later. When matched for saccade velocity, the time courses and magnitudes of postsaccadic facilitation for activity in the dark and during visual stimulation were identical. The presaccadic suppression observed in the dark condition was similar for X and Y cells, whereas the postsaccadic facilitation was substantially stronger for X cells, both in the dark and for visually evoked responses. This saccade-related regulation of geniculate transmission appears to be independent of the conditions under which the saccade is evoked or the state of retinal input to the LGN. The change in activity from presaccadic suppression to postsaccadic facilitation amounted to an increase in gain of geniculate transmission of approximately 30%. This may promote rapid central registration of visual inputs by increasing the temporal contrast between activity evoked by an image near the end of a fixation and that evoked by the image immediately after a saccade.     

Neuronal activity in the primate supplementary motor area and the primary motor cortex in relation to spatio-temporal bimanual coordination

Single neuronal activity was recorded from the supplementary motor area (SMA-proper and pre-SMA) and primary motor cortex (M1) in two Macaca fascicularis trained to perform a delayed conditional sequence of coordinated bimanual pull and grasp movements. The behavioural paradigm was designed to distinguish neuronal activity associated with bimanual coordination from that related to a comparable motor sequence but executed unimanually (left or right arm only). The bimanual and unimanual trials were instructed in a random order by a visual cue. Following the cue, there was a waiting period until presentation of a "go-signal", signalling the monkey to perform the instructed movement. A total of 143 task-related neurons were recorded from the SMA (SMA-proper, 62; pre-SMA, 81). Most SMA units (87%) were active in both unimanual contralateral and unimanual ipsilateral trials (bilateral neurons), whereas 9% of units were active only in unimanual contralateral trials and 3% were active only in unimanual ipsilateral trials. Forty-eight per cent of SMA task-related units were classified as bimanual, defined as neurons in which the activity observed in bimanual trials could not be predicted from that associated with unimanual trials when comparing the same events related to the same arm. For direct comparison, 527 neurons were recorded from M1 in the same monkeys performing the same tasks. The comparison showed that M1 contains significantly less bilateral neurons (75%) than the SMA, whereas the reverse was observed for contralateral neurons (22% in M1). The proportion of M1 bimanual cells (53%) was not statistically different from that observed in the SMA. The results suggest that both the SMA and M1 may contribute to the control of sequential bimanual coordinated movements. Interlimb coordination may then take place in a distributed network including at least the SMA and M1, but the contribution of other cortical and subcortical areas such as cingulate motor cortex and basal ganglia remains to be investigated.     

Eye-hand interactions during goal-directed pointing movements

Saccadic eye and hand movements made to step displacements in target position were measured under conditions designed to dissociate the output of the ocular and manual motor systems. This was accomplished by having subjects look and point, either with or without vision of the hand (closed or open loop, respectively) at peripheral targets starting from independent initial positions. The results showed that the amplitude of open loop pointing responses increased in size when accompanied by saccades that were larger than the required hand movement. Providing the subject with visual feedback of the hand during the response or asking them to visually fixate caused this effect to disappear. Taken together, this pattern of results suggests that when vision of the hand is unavailable the programming of saccade metrics influences the control of simultaneously produced pointing movements in an on-line manner.     

Role of the oculomotor vermis in generating pursuit and saccades: effects of microstimulation

We studied the eye movements evoked by applying small amounts of current (2-50 microA) within the oculomotor vermis of two monkeys. We first compared the eye movements evoked by microstimulation applied either during maintained pursuit or during fixation. Smooth, pursuitlike changes in eye velocity caused by the microstimulation were directed toward the ipsilateral side and occurred at short latencies (10-20 ms). The amplitudes of these pursuitlike changes were larger during visually guided pursuit toward the contralateral side than during either fixation or visually guided pursuit toward the ipsilateral side. At these same sites, microstimulation also often produced abrupt, saccadelike changes in eye velocity. In contrast to the smooth changes in eye velocity, these saccadelike effects were more prevalent during fixation and during pursuit toward the ipsilateral side. The amplitude and type of evoked eye movements could also be manipulated at single sites by changing the frequency of microstimulation. Increasing the frequency of microstimulation produced increases in the amplitude of pursuitlike changes, but only up to a certain point. Beyond this point, the value of which depended on the site and whether the monkey was fixating or pursuing, further increases in stimulation frequency produced saccadelike changes of increasing amplitude. To quantify these effects, we introduced a novel method for classifying eye movements as pursuitlike or saccadelike. The results of this analysis showed that the eye movements evoked by microstimulation exhibit a distinct transition point between pursuit and saccadelike effects and that the amplitude of eye movement that corresponds to this transition point depends on the eye movement behavior of the monkey. These results are consistent with accumulating evidence that the oculomotor vermis and its associated deep cerebellar nucleus, the caudal fastigial, are involved in the control of both pursuit and saccadic eye movements. We suggest that the oculomotor vermis might accomplish this role by altering the amplitude of a motor error signal that is common to both saccades and pursuit.     

Saccade latency toward auditory targets depends on the relative position of the sound source with respect to the eyes

The latency of saccadic eye movements evoked by the presentation of auditory and visual targets was studied while starting eye position was either 0 or 20 deg right, or 20 deg left. The results show that for any starting position the latency of visually elicited saccades increases with target eccentricity with respect to the eyes. For auditory elicited saccades and for any starting position the latency decreases with target eccentricity with respect to the eyes. Therefore auditory latency depends on a retinotopic motor error, as in the case of visual target presentation.     

An oculomotor representation area within the ventral premotor cortex

We explored the ventral part of the premotor cortex (PMV) with intracortical microstimulation (ICMS) while monkeys performed a visual fixation task, to see whether the PMV is involved in oculomotor control. ICMS evoked saccades from a small-restricted region in the PMV, without evoking movements in the limbs, neck, or body. We found the saccade-evoking site in the PMV in a total of three hemispheres in two monkeys. Quantitative analysis of the effects of eye position on saccades evoked by microstimulation of the PMV characterized the evoked saccades as goal directed. The nature of the saccades evoked in the PMV contrasted with the fixed vector nature of saccades evoked by ICMS of the frontal eye field. We also found that neurons in this restricted area of the PMV were active while the animals were performing a saccade task that required them to make saccades toward targets without arm movements. These data provide evidence for the presence of an oculomotor-specific subregion within the PMV. This subregion and the surrounding skeletomotor-representing regions of the PMV seem to coordinate oculomotor and skeletomotor control in performing goal-directed motor tasks.     

Movement sequence-related activity reflecting numerical order of components in supplementary and presupplementary motor areas

The supplementary motor area (SMA) and presupplementary motor areas (pre-SMA) have been implicated in movement sequencing, and neurons in SMA have been shown to encode what might be termed the relational order among sequence components (e.g., movement X followed by movement Y). To determine whether other aspects of movement sequencing might also be encoded by SMA or pre-SMA neurons, we analyzed task-related activity recorded from both areas in conjunction with a sequencing task that dissociated the numerical order of components (e.g., movement X as the 2nd component, irrespective of which movements precede or follow X). Sequences were constructed from eight component movements, each characterized by three spatial variables (origin, direction, and endpoint). Task-related activity recorded from 56 SMA and 63 pre-SMA neurons was categorized according to both the epoch (delay, reaction time, and movement time) and the spatial variable or component movement with which it was associated. All but one instance of task-related activity was selective for one of the spatial variables (SV-selective) rather than for any of the component movements themselves. Of 110 instances of SV-selective activity in SMA, 43 (39%) showed significant effects of numerical order. The corresponding incidence in pre-SMA, 82 (71%) of 116, was substantially higher (P < 0.00001). No effects of numerical order were evident among the hand paths, movement times, or electromyographic activity associated with task performance. We concluded that neurons in SMA and pre-SMA may encode the numerical order of components, at least for sequences that are distinguished mainly by that aspect of component ordering.     

Role for cells in the presupplementary motor area in updating motor plans

Two motor areas are known to exist in the medial frontal lobe of the cerebral cortex of primates, the supplementary motor area (SMA) and the presupplementary motor area (pre-SMA). We report here on an aspect of cellular activity that characterizes the pre-SMA. Monkeys were trained to perform three different movements sequentially in a temporal order. The correct order was planned on the basis of visual information before its execution. A group of pre-SMA cells (n = 64, 25%) were active during a process when monkeys were required to discard a current motor plan and develop a plan appropriate for the next orderly movements. Such activity was not common in the SMA and not found in the primary motor cortex. Our data suggest a role of pre-SMA cells in updating motor plans for subsequent temporally ordered movements.     

Saccadic gain modification: visual error drives motor adaptation

The brain maintains the accuracy of saccadic eye movements by adjusting saccadic amplitude relative to the target distance (i.e., saccade gain) on the basis of the performance of recent saccades. If an experimenter surreptitiously moves the target backward during each saccade, thereby causing the eyes to land beyond their targets, saccades undergo a gradual gain reduction. The error signal driving this conventional saccadic gain adaptation could be either visual (the postsaccadic distance of the target from the fovea) or motoric (the direction and size of the corrective saccade that brings the eye onto the back-stepped target). Similarly, the adaptation itself might be a motor adjustment (change in the size of saccade for a given perceived target distance) or a visual remapping (change in the perceived target distance). We studied these possibilities in experiments both with rhesus macaques and with humans. To test whether the error signal is motoric, we used a paradigm devised by Heiner Deubel. The Deubel paradigm differed from the conventional adaptation paradigm in that the backward step that occurred during the saccade was brief, and the target then returned to its original displaced location. This ploy replaced most of the usual backward corrective saccades with forward ones. Nevertheless, saccadic gain gradually decreased over hundreds of trials. Therefore, we conclude that the direction of saccadic gain adaptation is not determined by the direction of corrective saccades. To test whether gain adaptation is a manifestation of a static visual remapping, we decreased the gain of 10 degrees horizontal saccades by conventional adaptation and then tested the gain to targets appearing at retinal locations unused during adaptation. To make the target appear in such "virgin territory," we had it jump first vertically and then 10 degrees horizontally; both jumps were completed and the target spot extinguished before saccades were made sequentially to the remembered target locations. Conventional adaptation decreased the gain of the second, horizontal saccade even though the target was in a nonadapted retinal location. In contrast, the horizontal component of oblique saccades made directly to the same virgin location showed much less gain decrease, suggesting that the adaptation is specific to saccade direction rather than to target location. Thus visual remapping cannot account for the entire reduction of saccadic gain. We conclude that saccadic gain adaptation involves an error signal that is primarily visual, not motor, but that the adaptation itself is primarily motor, not visual.     

Visuospatial properties of ventral premotor cortex

In macaque ventral premotor cortex, we recorded the activity of neurons that responded to both visual and tactile stimuli. For these bimodal cells, the visual receptive field extended from the tactile receptive field into the adjacent space. Their tactile receptive fields were organized topographically, with the arms represented medially, the face represented in the middle, and the inside of the mouth represented laterally. For many neurons, both the visual and tactile responses were directionally selective, although many neurons also responded to stationary stimuli. In the awake monkeys, for 70% of bimodal neurons with a tactile response on the arm, the visual receptive field moved when the arm was moved. In contrast, for 0% the visual receptive field moved when the eye or head moved. Thus the visual receptive fields of most "arm + visual" cells were anchored to the arm, not to the eye or head. In the anesthetized monkey, the effect of arm position was similar. For 95% of bimodal neurons with a tactile response on the face, the visual receptive field moved as the head was rotated. In contrast, for 15% the visual receptive field moved with the eye and for 0% it moved with the arm. Thus the visual receptive fields of most "face + visual" cells were anchored to the head, not to the eye or arm. To construct a visual receptive field anchored to the arm, it is necessary to integrate the position of the arm, head, and eye. For arm + visual cells, the spontaneous activity, the magnitude of the visual response, and sometimes both were modulated by the position of the arm (37%), the head (75%), and the eye (58%). In contrast, to construct a visual receptive field that is anchored to the head, it is necessary to use the position of the eye, but not of the head or the arm. For face + visual cells, the spontaneous activity and/or response magnitude was modulated by the position of the eyes (88%), but not of the head or the arm (0%). Visual receptive fields anchored to the arm can encode stimulus location in "arm-centered" coordinates, and would be useful for guiding arm movements. Visual receptive fields anchored to the head can likewise encode stimuli in "head-centered" coordinates, useful for guiding head movements. Sixty-three percent of face + visual neurons responded during voluntary movements of the head. We suggest that "body-part-centered" coordinates provide a general solution to a problem of sensory-motor integration: sensory stimuli are located in a coordinate system anchored to a particular body part.     

A neural model of multimodal adaptive saccadic eye movement control by superior colliculus

How does the saccadic movement system select a target when visual, auditory, and planned movement commands differ? How do retinal, head-centered, and motor error coordinates interact during the selection process? Recent data on superior colliculus (SC) reveal a spreading wave of activation across buildup cells the peak activity of which covaries with the current gaze error. In contrast, the locus of peak activity remains constant at burst cells, whereas their activity level decays with residual gaze error. A neural model answers these questions and simulates burst and buildup responses in visual, overlap, memory, and gap tasks. The model also simulates data on multimodal enhancement and suppression of activity in the deeper SC layers and suggests a functional role for NMDA receptors in this region. In particular, the model suggests how auditory and planned saccadic target positions become aligned and compete with visually reactive target positions to select a movement command. For this to occur, a transformation between auditory and planned head-centered representations and a retinotopic target representation is learned. Burst cells in the model generate teaching signals to the spreading wave layer. Spreading waves are produced by corollary discharges that render planned and visually reactive targets dimensionally consistent and enable them to compete for attention to generate a movement command in motor error coordinates. The attentional selection process also helps to stabilize the map-learning process. The model functionally interprets cells in the superior colliculus, frontal eye field, parietal cortex, mesencephalic reticular formation, paramedian pontine reticular formation, and substantia nigra pars reticulata.