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Department of Psychology, Princeton University, Princeton, New Jersey 08544
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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Graziano, Michael S. A., Xin Tian Hu, and Charles G. Gross. Visuospatial properties of ventral premotor cortex. J. Neurophysiol. 77: 2268-2292, 1997. 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.
Premotor cortex, also called area 6, is thought to be involved in the planning and execution of movements (e.g., Kalaska and Crammond 1992
All husbandry, surgical, and behavioral procedures were approved by the Princeton University Institutional Animal Care and Use Committee and the consultant veterinarian and were in accordance with National Institutes of Health and U.S. Department of Agriculture guidelines.
Initial surgery
For each monkey, an initial surgical operation was performed under deep pentobarbital sodium anesthesia and strict aseptic conditions, during which the top of the skull was cleared of skin and muscle, titanium screws were screwed into the bone, and the exposed bone was covered with a layer of dental acrylic ~1 cm thick. A stainless steel recording chamber, 2.5 cm diam, was embedded in the acrylic over the frontal lobe for a vertical approach to PMv. A steel bolt for holding the head was also embedded in the acrylic. For monkeys 2 and 3 the conjunctiva of one eye was cut open, a scleral eye coil was inserted, and the incision was sutured closed again. The leads to the eye coil were passed under the skin to an electrical connector embedded in the acrylic implant. Each animal recovered from the effects of the surgery within several days, but was given three additional weeks to allow the skull to grow tightly around the skull screws.
Anesthetized recording procedures
At the beginning of each recording session, the animal was given an intramuscular injection of atropine sulfate (0.15 mg/kg) to reduce mucosal secretions, and then given a restraining dose of ketamine hydrochloride (10 mg/kg) with acepromazine (0.4 mg/kg). The animal was then intubated with a pediatric tracheal tube coated with 2% xylocaine jelly and given a 2:1 mixture of nitrous oxide and oxygen to which 2.5% halothane was added. The head was then fixed into a stereotaxic frame by means of the head bolt. This technique eliminated the need for ear bars and eye bars, and therefore there were no pressure points in the ear canals or orbits. The animal rested on heating pads wrapped in towels, and its body temperature was maintained at 37-38°C. Electrocardiogram was continuously monitored through skin electrodes. The animal was immobilized with an intravenous infusion (0.03 mg·kg Awake recording procedures
During the daily recording sessions, the monkey's head was held in place by the head bolt and a hydraulic microdrive was mounted to the top of the recording chamber. A steel guide cannula (an 18-ga. syringe needle) was lowered through the hole in the skull and into the dura. Then the varnish-coated tungsten microelectrode (Frederick Haer, impedance 0.5-5 M Stimuli
Once a cell was isolated, as indicated by the repeatability of its wave form on the oscilloscope, it was tested with a standard battery of stimuli. Somatosensory responsiveness was studied with the use of manual palpation, manipulation of joints, gentle pressure, and stroking with cotton swabs. Somatosensory receptive fields were plotted by repeated presentation of the most effective of these stimuli. Responses on the face were tested while the eyes were covered.
Behavioral training: monkeys 2 and 3
Each animal was trained by means of fruit rewards to climb out of the home cage and to sit in a primate chair. The animal was restrained in the chair by a rigid Plexiglas collar bolted to the sides of the chair. The monkey was then trained to extend one arm, allowing the arm to be strapped down with Velcro strips to a metal arm holder. The head was held in place by the head bolt. During 4-h daily sessions over several weeks, the animal was trained to sit quietly while restrained in this manner and while being touched with cotton swabs on the face, around the eyes, or on other parts of the body. Visual stimuli (described below) were mounted on the end of the robot arm and moved toward and away from the face until the monkey became fully accustomed to them and ignored them. This lack of any visible motor response to the visual stimuli was crucial for the experiment, because many neurons in PMv respond during voluntary movement.
Behavioral paradigm for arm + visual cells in the awake monkey
The monkey sat with the head fixed by the head bolt and the arm contralateral to the recording electrode strapped to an arm holder with Velcro strips (see Fig. 5, top). The arm holder could be adjusted to different positions. Three LEDs were spaced 20° apart along the horizontal meridian at eye level and positioned 28.5 cm in front of the monkey. Each trial began with one of the LEDs turning on and blinking at a frequency of 4 Hz. As soon as the animal fixated the LED within a 5°-diam window, the blinking stopped and the LED remained on. If the animal maintained fixation for the remainder of the trial (randomly varied between 1.2 and 1.5 s), the LED would turn off, a valve would release ~0.2 ml of juice into the animal's mouth, and the 10-s intertrial interval would commence. If the animal broke fixation at any time during the trial, the LED was extinguished, no reward was given, and the intertrial interval would commence. As described above, the monkey fixated within 1° of the fixation spot, much better than the required 5°.
Behavioral paradigm for face + visual cells in the awake monkey
The task used for testing face + visual cells was the same as the one described above for testing arm + visual cells, except as follows. The monkey fixated one of three lights, FIX A, FIX B, or FIX C, spaced 15° apart horizontally and positioned ~20° below eye level. During fixation, the visual stimulus (usually a ping-pong ball, sometimes a cotton swab) was advanced toward the monkey for 1 s at 10 cm/s along one of five trajectories (see Fig. 13, top). These trajectories were arranged at eye level. The three eye positions and five stimulus positions yielded 15 conditions, which were presented in an interleaved fashion, usually 10 trials per condition. In separate blocks of trials, the monkey's head was fixed straight (shown), or rotated 15° to the right or the left. The arm contralateral to the recording electrode was fixed straight ahead or bent across the chest.
Statistical procedures
The experiments on arm + visual neurons used a 4 × 3 × 2 × 2 factorial design (4 stimulus trajectories × 3 eye positions × 2 arm positions × 2 data collection periods, the prestimulus period and the stimulus period). The experiments on face + visual neurons used a 5 × 3 × 2 × 2 design (5 stimulus trajectories × 3 eye positions × 2 head positions × 2 data collection periods). Many neurons were only tested on some conditions, and in these cases an overall analysis of variance (ANOVA) was impossible. In any case, our specific hypotheses would not have been addressed by examining the main effects or interaction terms in an overall ANOVA, but could only be addressed by specific comparisons. Therefore for each neuron we performed four types of specific comparisons (described below). The level of t-TEST FOR VISUAL RESPONSE.
Neuron S86 responded to stimulus trajectory IV (see Fig. 5, bottom, row A1). To test the significance of this response, we compared the mean spikes per second in the prestimulus period to the mean spikes per second in the stimulus period with the use of a paired t-test. The result was significant (t = 10.18, P < 0.05). Neurons that did not respond significantly to at least one trajectory were not analyzed further.
CONTRAST ANALYSIS FOR MOVEMENT OF VISUAL RESPONSE.
In Fig. 5, row A1, the visual response was best at trajectory IV. In contrast, in row A2, the visual response was best at trajectory III. That is, when the arm moved, the visual receptive field also moved. To test whether this movement was significant, a standard contrast analysis was used (Rosenthal and Rosnow 1985 ANOVA FOR MODULATION OF RESPONSE MAGNITUDE.
The visual response to trajectory IV is larger in Fig. 5, row A1 than in rows B1 or C1. That is, the position of the eye may have modulated the magnitude of the visual response. Note that we consider only the stimulus trajectory that gave the best response. This selection is necessary to avoid analyzing the spontaneous activity represented by the nonresponding positions. (As described below, a separate method was used to test for modulation of spontaneous activity.) To characterize the amount of modulation, we calculated the percent change in response between row A1, trajectory IV (eye position with highest response), and row B1, trajectory IV (eye position with lowest response). We used the following formula: % change = 100 × (response at best eye position ANOVA FOR MODULATION OF SPONTANEOUS ACTIVITY.
We also tested whether the spontaneous activity of the neuron (the activity in the prestimulus period) was modulated by the position of the eyes. We first calculated the percent change in spontaneous activity by the use of the formula: % change = 100 × (mean spontaneous activity at best eye position Active and passive movement of the head
To study the effect of head movement, we loosened the clamp on the head bolt, allowing the head to turn freely side to side but not in any other direction. In the active movement condition, the monkey made frequent spontaneous head movements while we recorded single neuron activity. In the passive movement condition, the experimenter stood behind the monkey, grasped the head bolt with a pair of pliers, and turned it. To measure the head position, we used a 15-mm-diam coil of insulated wire (Cooner Wire, 15 strand, No. AS632), similar to the eye coil, but attached directly to the acrylic implant. An oscillating magnetic field was used to induce a current in the wire coil, which was measured at a sampling rate of 50 Hz (C-N-C Engineering, Dual Power Oscillators, 3-ft-diam magnetic coils).
Histology
At the completion of the experiment, monkeys 1 and 2 were given an overdose of pentobarbital sodium (100 mg/kg) and perfused transcardially with saline and then 10% Formalin. The head was put in a stereotaxic apparatus, the skull was opened, and the brain was exposed. The positions of the arcuate and central sulci were measured stereotaxically. Figure 1 shows the entry locations of the electrode penetrations in relation to the sulci for monkey 1. Most recording sites were within the posterior portion of PMv, on the cortical surface, in an area that Rizzolatti and colleagues have termed F4 (Gentilucci et al. 1988 Response categories
We studied 604 neurons in PMv in four hemispheres of three monkeys. Monkey 1 was studied under anesthesia and monkeys 2 and 3 were studied while awake and fixating. Neuronal responses were classified as somatosensory, visual, bimodal (somatosensory + visual), or auditory. In the awake preparation, we were also able to test activity related to the monkey's spontaneous movements. Table 1 shows the proportions of these different response types. Thirty-one percent of the neurons were classified as bimodal, and are the main focus of this paper.
Somatotopic organization
Most of the neurons that we studied in PMv (409 of 604, 68%) responded to somatosensory stimuli. These neurons were somatotopically organized. As shown in Fig. 1 for monkey 1, studied under anesthesia, when electrode penetrations were made in the medial part of PMv, near the genu of the arcuate sulcus, the somatosensory receptive fields were usually located on the arm (labeled A) or hand (labeled H). When penetrations were made a few millimeters laterally, the tactile receptive fields were usually located on the face (labeled F) or inside the mouth (labeled M). A similar somatotopic organization was found in monkey 3, tested while the monkey was awake. In monkey 2, however, we did not record from enough locations in PMv to test the somatotopic organization.
Bimodal responses
A typical example of a bimodal, somatosensory + visual cell, studied in the anesthetized preparation, is illustrated in Fig. 2A. The tactile receptive field was plotted while the animal's eyes were covered. The cell was activated by lightly touching the facial hair, and the responsive region covered most of the contralateral cheek and the area around the mouth. When the animal's eyes were uncovered, the response began as the stimulus (a cotton swab) approached the face, but before it had touched. By approaching the face from various angles, we determined the three-dimensional structure of the visual receptive field. The boxed region in Fig. 2A shows the region of greatest response, a solid angle centered at the tactile receptive field and extending out ~10 cm. Outside of this region, the response was weak and erratic, grading into spontaneous activity at a distance of ~20 cm from the face. The visual response was not caused by inadvertent tactile stimulation, such as by air movement or static electricity, because it was eliminated by covering the eyes. The cell gave no response to conventional visual stimuli, such as bars of light projected onto a tangent screen, colored bars of light, or expanding or contracting squares of light. The shape, color, motion, or texture of the object placed near the face did not affect the response. If a stimulus was held stationary near the face, the cell responded in a sustained fashion for
Selectivity for the direction of stimulus motion
We used the following paradigm to test the directional selectivity of bimodal neurons in the awake preparation. While the animal fixated, a ping-pong ball mounted on the end of the robot arm was moved for 0.5 s at 10 cm/s along one of six possible trajectories, arranged such that their midpoints intersected ~20 cm in front of the monkey. The directions of motion were as follows: toward, away, left, right, up, and down. These stimulus trajectories were presented in an interleaved fashion, usually 10 trials per condition.
Selectivity for the distance to the stimulus
Figure 4 shows the responses of a typical bimodal neuron studied in the awake preparation. The cell had a bilateral tactile receptive field on the eyebrows and a bilateral visual receptive field. Figure 4A, top histogram, shows the result when a 2 × 2 cm white cardboard square, mounted on the robot arm, was advanced toward the face from a distance of 37.5 cm to a distance of 2 cm, over 4.3 s. The monkey did not fixate during this period because the stimulus would have blocked the fixation LED from view. (As described below, the magnitude and specificity of the visual response is as good or better when the animal is not fixating.) At the onset of stimulus motion, the cell gave a transient response and then returned to its baseline activity. When the stimulus had approached within ~25 cm of the face, the cell began to respond again. This response increased as the stimulus neared the face. When the stimulus stopped moving, the firing rate dropped but still remained well above baseline.
Visual receptive fields that move with the arm but not the eye or head
In this section we present the results for arm + visual neurons studied in the awake preparation. As described in METHODS, the monkey fixated one of three lights, FIX A, FIX B, or FIX C, while the visual stimulus was advanced along one of four trajectories, I-IV (Fig. 5, top). The arm contralateral to the recording electrode was strapped to an arm holder and positioned on the right (contralateral) or bent toward the left (ipsilateral). The cross-hatching on the arm shows the location of the tactile receptive field for one arm + visual neuron. The responses of this neuron to the visual stimulus are shown in Fig. 5, bottom.
Visual receptive fields that move with the head, not with the eye or the arm
To test whether cells with tactile responses on the face had head-centered visual receptive fields, we varied the position of the head, the arm, and the eyes. The monkey fixated one of three lights, FIX A, FIX B, or FIX C, spaced 15° apart horizontally (Fig. 13, top). During fixation, the visual stimulus was advanced toward the monkey along one of the five trajectories shown (I-V).
Responses during voluntary movement of the head
We recorded from face + visual neurons while the monkey turned its head to the right or the left, or reached with the contralateral arm toward pieces of fruit. Of the 27 face + visual neurons tested in this fashion, none responded in association with movements of the arm. In contrast, 17 (63%) responded significantly above baseline as the monkey turned its head (t-test, P < 0.05).
Visual and tactile responses in premotor cortex
We studied the sensory properties of neurons in PMv, both in the anesthetized and in the awake macaque. The recording sites were located on the cortical convexity posterior to the arcuate sulcus, corresponding mainly to area F4 as defined by Rizzolatti and colleagues (Gentilucci et al. 1988 Motor versus sensory response
The neuronal activity during stimulus presentation might not be sensory at all, but instead might represent the monkey's attempt to flinch. Indeed, a large proportion (32%) of the neurons in the awake preparation responded during voluntary movements of the arm, mouth, or head.
Coding of space in body-part-centered coordinates
In most visual areas of the brain, the cells encode the locations of visual images on the retina, that is, in retinocentric coordinates. When the eye moves, the visual receptive fields also move. For most of the bimodal, visual-tactile neurons in PMv, however, the visual receptive fields were not anchored to the retina. Instead, we found that most bimodal cells with a tactile response on the arm had a visual receptive field that was anchored to the arm; and most bimodal cells with a tactile response on the face had a visual receptive field that was anchored to the head. These cells can therefore encode the locations of visual stimuli with respect to the arm, that is, in "arm-centered" coordinates, or with respect to the head in head-centered coordinates. We expect that neurons in a more dorsal part of premotor cortex, in a possible leg representation (Kurata 1989 Possible functions of the tactile receptive fields: locating stimuli in space
If bimodal neurons in PMv encode the visual space near the body, then what is the function of their tactile responses? The tactile and visual receptive fields of a bimodal neuron are continuous, detecting the presence of a stimulus anywhere within the critical region of space. A strictly tactile neuron has a spatial receptive field that extends only a short distance from the skin, ~1 cm, the length of the hair. A bimodal neuron has a spatial receptive field that may extend farther from the body, in some cases beyond a meter. This range of receptive fields would be useful for encoding the distance from the body part to the stimulus.
Possible functions of the tactile receptive fields: ontogeny of spatial perception
One of the central puzzles in cognitive development is how an infant learns to interpret patterns of light on the retina as a three-dimensional space and how it learns to use that information to guide movement (e.g., Epstein and Rogers 1995 Visual guidance of movement
We suggest that body-part-centered receptive fields provide a general solution to a central problem of sensory-motor integration (Graziano and Gross 1994 Modulation of the response magnitude by the position of the eye, arm, and head: a possible mechanism for computing body-part-centered coordinates
Andersen and colleagues (Andersen and Mountcastle 1983 Interconnected system of bimodal areas
Several other areas of the macaque brain contain bimodal, visual-tactile neurons that are strikingly similar to the bimodal neurons in PMv. These areas include area 7b in the posterior parietal lobe, VIP, which lies on the floor of the intraparietal sulcus, and the putamen. Area 7b, VIP, and PMv are monosynaptically interconnected, and all three project to the putamen (Cavada and Goldman-Rakic 1989a PUTAMEN.
Most neurons in the monkey putamen respond to a touch on the skin, rotation of the joints, or deep muscle pressure, and many will respond only when the animal makes a voluntary movement (e.g., Alexander 1987 VIP.
Colby et al. (1993) AREA 7B.
Neurons in area 7b respond to somatosensory stimuli such as touch, deep pressure, joint rotation, and pain (Dong et al. 1994
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Wise 1985). It projects in a topographic fashion to primary motor cortex (M1) and also directly to the spinal cord (Barbas and Pandya 1987; Dum and Strick 1991; Godschalk et al. 1984; He et al. 1993; Leichnetz 1986; Matelli et al. 1986; Matsumura and Kubota 1979; Muakkassa and Strick 1979). Premotor neurons are active during specific voluntary movements, and electrical stimulation of different parts of the somatotopic map will evoke muscle movement in the corresponding part of the body (Caminiti et al. 1990; Gentilucci et al. 1988; Hepp-Raymond et al. 1994; Weinrich et al. 1984).
). The visual areas 7a, lateral intraparietal area (LIP), ventral intraparietal area (VIP), and medial superior temporal area (MST) all project to area 7b, which in turn projects to premotor cortex, mainly to the ventral half (Cavada and Goldman-Rakic 1989a,b; Jones and Powell 1970; Kunzle 1978; Matelli et al. 1986; Mesulam et al. 1977). This ventral region (see Fig. 1) has several names, including ventral premotor cortex (PMv), 6Va, and PMa (see He et al. 1993). Here we refer to it as PMv.
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FIG. 1.
Top: location of ventral premotor cortex (PMv; shaded area) on side view and top view of macaque monkey brain. Bottom: top view of arcuate sulcus and PMv in an anesthetized monkey, showing somatotopic organization. Black dots: locations of electrode penetrations for which the tactile receptive fields were located on the arm (A), hand (H), face (F), or inside of the mouth (M). Underlines: penetrations on which bimodal, visual-tactile cells were located. One penetration first entered cortex anterior to the arcuate sulcus, but then continued into PMv in the posterior bank of the sulcus. Three posterior penetrations were presumably in motor cortex (M1). Because the electrode penetrations were not perpendicular to the cortical surface, deeper recordings were sometimes at a different somatotopic location than superficial recordings. Therefore only responses within 1 mm of the surface are included here. Seven penetrations, for which no responses were found in the 1st mm, are not shown.
; Matelli et al. 1986; Muakkassa and Strick 1979). Many of these tactile neurons also respond when a visual stimulus is placed in the region of space near the tactile receptive field (Fogassi et al. 1996; Gentilucci et al. 1988; Rizzolatti et al. 1981). Such bimodal neurons are especially numerous in the posterior part of PMv, which Gentilucci et al. (1988) have termed area F4.
; Gentilucci et al. 1983) found that the bimodal, visual-tactile neurons in PMv behaved in a different fashion. For most PMv neurons, when the eye moved, the visual receptive field did not move. Instead, it remained in the same region of space, near the tactile receptive field. Fogassi et al. (1992) suggested that these visual receptive fields may be anchored to the head, or possibly to the body, rather than to the retina. According to this hypothesis, visual space is encoded in PMv in "head-centered" or "body-centered" coordinates. The hypothesis, however, was not directly tested. Although the visual receptive fields did not move with the eye, and therefore were not anchored to the retina, they might have been anchored to the head, the chest, the arm, the leg, or even to an external landmark such as the frame of the primate chair.
; Graziano et al. 1994).
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
1·h1) of pancuronium bromide (Pavulon) through a pediatric intravenous cannula and was artificially respired. Respiratory rate and volume were adjusted to give an end-tidal carbon dioxide level of 3.5-4.5%. The pupils were dilated with cyclopentolate (Cyclogyl, 1%), and the corneas were covered with contact lenses selected to focus the eyes on a rear projection tangent screen. The cap of the recording chamber was removed, exposing the dura. Halothane was then discontinued, and the animal was maintained under 2:1 nitrous oxide and oxygen. No surgery or potentially painful procedures were performed after the halothane was discontinued.
) was advanced through the cannula and into the brain. There was no change in heart rate from the introduction of the guide cannula or the electrode, suggesting that the animal felt no pain under these conditions. Stimuli applied to the animal during the experiment, such as touching the skin, manipulating or gently squeezing the limbs, and moving objects toward or away from the face, also caused no change in heart rate. In control tests, when the animal was respired with 2:1 nitrous oxide and oxygen but not immobilized with Pavulon, there were no motor signs of distress as a result of these visual and somatosensory stimuli.
.)
) was advanced from the guide cannula into the brain, to record from neurons in the cortex immediately below the dura. We believe that the stability of the electrode and the guide tube was markedly enhanced by the use of a narrow hole through the acrylic and skull. This procedure not only reduced the heartbeat pulsation of the brain, but also allowed a column of tough connective tissue to fill the entire 1-cm-deep, 2-mm-wide hole, thus forming a matrix to stabilize the guard tube. This stability was particularly important in experiments in which the head bolt was loosened and the animal was allowed to turn its head freely from side to side. Even sudden head movements did not displace the electrode enough to interfere with single-neuron recording. (For a more detailed description of some of the awake recording procedures, see Rodman 1991).
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FIG. 5.
Top: experimental paradigm for testing the effect of arm position. On each trial the animal fixated 1 of 3 lights spaced 20° apart (FIX A, FIX B, or FIX C) and the stimulus was advanced along 1 of 4 trajectories (I-IV). The arm was fixed in 1 of 2 positions. Trajectories and monkey are drawn to the same scale. Stippling: tactile receptive field (RF) of the cell whose responses are illustrated at bottom. Bottom: histograms of neuronal activity, summed over 10 trials, as a function of eye position (A-C), stimulus position (I-IV), and arm position (to the right in rows A1, B1, and C1, and to the left in row A2). Vertical lines: stimulus onset. When the arm was fixed to the right, the neuron responded best to the rightmost stimulus trajectory (IV), whether the eye looked to the left (as in row A1), to the center (as in row B1), or to the right (as in row C1). However, when the arm was fixed to the left (row A2), the neuron responded best to stimulus trajectory III. That is, the visual receptive field moved toward the left with the tactile receptive field. Results for conditions B2 and C2, not shown, were similar.
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FIG. 13.
Top: experimental paradigm for testing the effect of head, arm, and eye position. The monkey fixated 1 of 3 lights (FIX A, FIX B, or FIX C) spaced 15° apart. The stimulus was presented along 1 of 5 trajectories (I-V). The trajectories and the monkey are drawn to the same scale. The monkey's head was held straight (shown), or rotated 15° to the right or the left. The arm was strapped to a movable holder and held straight ahead or bent rightward across the chest. Black dot: hemisphere recorded from. Stippling: tactile receptive field of the cell whose responses are illustrated beneath. Bottom: histograms of neuronal activity, summed over 10 trials, as a function of eye position (FIX A, FIX B, FIX C), stimulus position (I-IV), arm position (to the right in row B2, to the left in all other conditions), and head position (to the right in row B3, straight in all other conditions). Vertical lines: stimulus onset. When the head was straight (rows A1, B1, C1, and B2), the neuron responded best to stimulus trajectory II, regardless of eye or arm position. When the head was rotated 15° to the right (row B3), the neuron responded best to trajectory III. Thus the visual receptive field moved toward the right with the head. The spontaneous activity was greatest when the eyes were angled 15° to the left of the head (rows A1 and B3).
was adjusted to compensate for the number of comparisons, with the use of the following approximation: we assumed that the "experimentwise error rate" = 1 
(1 )N, where N = the number of comparisons performed on that neuron. We then adjusted until the experimentwise error rate was 0.05. This method provides a relatively conservative test for significance (Linton et al. 1975). Because of the nature of the specific comparisons (e.g., ANOVAs on subsets of the data), it was not possible to use the other methods of controlling the level that are generally used on simple pairwise comparisons.
). The four means in row A2 were compared with a pattern of weights derived from the means in row A1. This specific comparison showed a significant match (Fmatch = 31.89, P < 0.01), but also a significant residual, or nonmatching, variance (Fresidual = 50.79, P < 0.01). That is, the pattern of response in row A1 significantly overlapped the pattern in row A2 (reflected in the significance of Fmatch), but the two patterns also had significant differences (reflected in the significance of Fresidual). To show that the visual receptive field shifted significantly, it is sufficient to show the significance of Fresidual. Therefore, in this case, the visual receptive field moved significantly with the arm.
response at worst eye position)/response at worst eye position. In this case, the change was 18%. To test the statistical significance of the modulation, we analyzed the response to trajectory IV with the use of a one-factor ANOVA with 3 levels (Fig. 5, rows A1, B1, and C1). The result, however, was not significant (F = 0.59, P > 0.05). Thus, for this neuron, the position of the eye did not modulate the magnitude of the visual response.
mean spontaneous activity at worst eye position)/mean spontaneous activity at worst eye position. In this case, the change was 27%. To test the statistical significance of the change, we analyzed the prestimulus period with the use of a 4 × 3 ANOVA (4 stimulus positions × 3 eye positions, conditions A1, B1, and C1). The main effect of eye position for cell S86 was not significant (F = 0.17, P > 0.05), indicating that eye position did not affect the magnitude of the spontaneous activity.
mean spontaneous activity at worst arm position)/mean spontaneous activity at worst arm position. In this case the change was 25%. We then analyzed the prestimulus activity with the use of a 4 × 2 ANOVA (4 stimulus positions × 2 arm positions, conditions A1 and A2). There was no significant main effect of arm position (F = 3.43, P > 0.05); thus the spontaneous activity of this cell was not significantly modulated by arm position.
; Rizzolatti et al. 1988). Some sites entered the cortex anterior to the arcuate sulcus and then passed into the posterior bank, into a region of PMv that Rizzolatti et al. have termed F5. Several penetrations were also made just anterior to the central sulcus, within 1 mm of the sulcus, presumably in M1.
). Vitamin E pills were glued to the monkey's scalp at several stereotaxic reference points. Because vitamin E is visible in the MRI scan, we were able to use these reference points to estimate the stereotaxic location of the arcuate sulcus. Some of the skull holes were also visible in the MRI, thus confirming that they were positioned directly over PMv, that is, just posterior to the lower limb of the arcuate sulcus.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
View this table:
TABLE 1.
Categories of neurons in the anesthetized and awake preparations
2 = 6.91,P < 0.01).
15 s, although we did not test longer than that. Presumably the response would have habituated eventually, because parts of the stereotaxic apparatus near the face did not elicit a response, judging by the cell's near-zero spontaneous activity.
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FIG. 2.
Six examples of bimodal, visual-tactile neurons from PMv. A-D were studied in the anesthetized preparation. E and F were studied in the awake preparation. The tactile receptive fields (cross-hatched) and the visual receptive fields (boxed) matched in location. Dotted line: visual receptive field extended beyond 1 m from the monkey. Black wedges (e.g., in A) and dots (e.g., in B): hemisphere recorded from. Arrows in B: preferred direction for tactile and visual stimuli. Curved arrow in E: preferred direction for both tactile and visual stimuli.
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FIG. 3.
Responses of 3 bimodal PMv neurons (rows A-C) to 6 different directions of stimulus movement. Each histogram is based on 10 trials. Vertical lines: time of stimulus onset. The stimulus moved at 10 cm/s for 0.5 s (indicated by the horizontal lines).
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FIG. 4.
Responses of a bimodal neuron from PMv with a tactile receptive field on the eyebrows. Each histogram is based on 10 trials. Stimuli were presented while the monkey was not performing the fixation task. In A-C the visual stimulus was advanced toward the face from in front at 8.25 cm/s and retracted on alternate trials. Stimulus farpoint = 37.5 cm, nearpoint = 2 cm, intertrial interval = 10 s. Vertical lines: onset and offset of stimulus movement. In A, the stimulus was a 2 × 2 cm square of cardboard viewed binocularly. The cell responded better as the stimulus approached. In B, 1 eye was covered, but the cell was still sensitive to depth. The baseline activity increased because the eye cover touched the tactile receptive field. In C, the stimulus was a 4 × 4 cm square of cardboard viewed binocularly. The increase in stimulus size did not cause a corresponding increase in response. In D, stationary stimuli were tested at 8 different distances. The cell still preferred nearby stimuli, even though all motion cues for depth had been eliminated. Error bars: means ± SE. Each point is based on 10 trials.
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FIG. 6.
Responses of a bimodal PMv neuron with a tactile receptive field that covered the entire contralateral arm. When the arm was fixed to the right (rows A1, B1, and C1), the visual response was strongest at trajectory IV, near the arm. The response remained at position IV despite the change in eye position (FIX A, FIX B, and FIX C). When the arm was extended leftward, the visual receptive field also extended leftward, to trajectories II and III. See also legend to Fig. 5.
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FIG. 7.
Responses of a bimodal PMv neuron with a tactile receptive field on the contralateral elbow. The visual receptive field remained in the same location whether the eyes fixated light A, B, or C. However, the magnitude of the visual response was modulated by eye position. The response was significantly greater when the eyes fixated light C. The contralateral arm was fixed to the right during these tests. See also legend to Fig. 5.
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FIG. 8.
Responses of a bimodal PMv neuron with a tactile receptive field on the contralateral arm. The visual response was strongest to trajectory IV, independent of the position of the eyes (rows A1, B1, or C1) or of the head (row A2). However, the activity of the neuron was modulated by the position of the head. Both the response and the spontaneous activity were reduced when the head was turned to the left. See also legend to Fig. 5.
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FIG. 9.
Responses of a bimodal neuron with a tactile receptive field on the right forearm. In rows C1 and C2, the fixation light-emitting diode (LED) was illuminated at the beginning of the trial and then extinguished during the presentation of the stimulus. The monkey was required to maintain fixation on the unilluminated LED until the end of the trial. When the arm was bent toward the left (row C2), the visual response moved with the arm toward the left. In rows NF1 and NF2, the fixation light was never illuminated and the monkey was not required to fixate. The response increased, and the movement of the visual receptive field with the arm was more pronounced.
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FIG. 10.
Responses of a bimodal PMv neuron with a tactile receptive field on the upper medial surface of the arm. When tested with hand-held stimuli, the cell responded best to visual stimuli within ~10 cm of the tactile receptive field. This visual receptive field moved when the arm was moved, remaining attached to the upper arm. However, the 4 robotic stimulus trajectories were not adequate to test this visual receptive field. When the arm was fixed on the right (row C1), the neuron responded to trajectory III. When the arm was fixed on the left (row C2), the visual receptive field was blocked by the arm, and the neuron no longer responded strongly to the stimuli presented by the robot.
View this table:
TABLE 2.
Bimodal neurons
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FIG. 11.
A: mean responses of the 19 arm + visual neurons for which the visual receptive field moved significantly with the arm. Responses are expressed as % of the maximum response for each neuron. Error bars: means ± SE. Visual receptive fields plotted while the arm was fixed on the right ( 
) have had their peaks aligned on the arrow, at position 4. When the arm was fixed to the left, the visual receptive fields moved to the left (
). B: mean responses of the 8 arm + visual neurons for which the visual response to the robot did not move significantly with the arm. For 5 of these 8 neurons, when the arm moved, the visual receptive field shifted out of the range of the robotic stimuli. When the cells were tested with hand-held stimuli, the visual receptive fields did move with the arm.
) have been aligned on the position marked by the arrow. If the visual receptive fields were retinocentric, as they are in most visual areas, then the data for the left-hand fixation (×) should be shifted toward the left of the arrow, and the data for the right-hand fixation () should be shifted toward the right of the arrow. Instead, all three curves fall at the same location. The entire population of receptive fields, therefore, remained stationary in space when the eyes moved.
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FIG. 12.
Mean responses of all 31 arm + visual neurons tested with 3 eye positions. Visual receptive fields plotted while the eye fixated the central position (FIX B, ) have had their peaks aligned on the arrow, at position 4. When the eye fixated 15° to the left (FIX A) or 15° to the right (FIX C), the visual receptive fields remained in the same location. That is, the visual receptive fields did not move as the eye moved. Responses are expressed as percents of the maximum response for each neuron. Error bars: means ± SE.
; Graziano et al. 1994).
, 1996) that such modulation of activity in PMv neurons is not caused by the position of the eye per se, but rather caused by the tension in the neck muscles, which is known to vary depending on the angle of gaze. According to this hypothesis, the purpose of the modulation is to encode the position of the head on the trunk. However, this hypothesis cannot be true for the example in Fig. 13. The activity of the neuron is clearly modulated by the position of the eye in the orbit, not by the position of the head on the trunk. In row A1, the head is straight and the eyes are 15° to the left. In row B3, the head has been rotated to the right, but the eyes are still at the same orbital position, that is, 15° to the left with respect to the head. Despite this change in head position, there is no significant change in spontaneous activity (8% change, F = 0.78, P > 0.05).
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FIG. 14.
Responses of a bimodal PMv neuron with a tactile receptive field on the contralateral snout. When the head was rotated 15° to the left (row B1), the neuron responded best to trajectory I. When the head was straight (row B2), the response was best to trajectory II. When the head was rotated 15° to the right (row B3), the response moved to trajectory III. Thus the visual receptive field was anchored to the head and moved as the head moved.
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FIG. 15.
Responses of a bimodal PMv neuron with a tactile receptive field on the contralateral snout and a visual receptive field that moved partly with the eyes and partly with the head. When the eyes fixated location A, the neuron responded best to trajectory II. When the eyes fixated location B, the neuron responded best to trajectory III. However, when the eyes fixated location C, the cell still responded best to trajectory III. When the head was rotated 15° to the right (compare rows B1 and B2), the visual receptive field did not move by the full amount that the head moved.
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FIG. 16.
Mean responses of all 20 face + visual neurons tested with multiple head positions. Visual receptive fields plotted while the head was straight ( ) have had their peaks aligned on the arrow, at 0°. When the head was rotated 15° to the right, the visual receptive fields also shifted an average of 15° to the right (). Responses are expressed as % of the maximum response for each neuron. Error bars: SE. Of these 20 neurons, 4 were also tested by rotating the head toward the left, and in these cases the visual receptive fields moved to the left with the head in a similar fashion.
), the right-hand position (×), or the left-hand position (), the population of visual receptive fields remained in the same location. That is, the population of cells coded visual space with respect to the head, not with respect to the eye.
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FIG. 17.
Mean responses of all 20 face + visual neurons tested with 3 eye positions. Visual receptive fields plotted while the eye fixated the central spot (FIX B, ) have had their peaks aligned on 0°. When the eye fixated location A, 15° to the left, or location C, 15° to the right, the visual responses remained in the same location. That is, the visual receptive fields did not move with the eyes. Responses are expressed as % of the maximum response for each neuron. Error bars: SE.
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FIG. 18.
Responses of a bimodal PMv neuron to active and passive rotation of the head. A: tactile receptive field (black shading: region of strongest response; gray shading: region of weaker response) and the visual receptive field (outlined) are strongest on the left side of the face. B: head bolt was loosened and the animal turned its head freely side to side. Downward direction of the trace: rightward head movement. Upward direction of the trace: leftward head movement. Vertical lines above trace: neuronal discharges. The neuron responded as the head turned toward the right, away from the visual receptive field. C: head was turned passively and the neuron no longer responded during the movement.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
; Rizzolatti et al. 1988). We found that the cells responded to somatosensory stimuli, visual stimuli, or both, i.e., were bimodal. In addition, many neurons in the awake monkey (32%) responded during voluntary movement.
; Gentilucci et al. 1988; Rizzolatti et al. 1981).
also found bimodal neurons in the hand representation of M1. Because PMv projects directly to M1, it is not surprising to find at least some bimodal neurons in M1.
). Both the tactile and visual responses had delimitable receptive fields that varied from one cell to the next. In the case of the visual responses, the receptive fields were not only confined in their angular spread, but also in their distance from the monkey. Some neurons responded only to stimuli within centimeters of the body, whereas others responded to stimuli >1 m away. It is unlikely that the monkey would flinch only to near stimuli, and then when the electrode had advanced to the next cell, suddenly change strategy and flinch to more distant stimuli as well. Similarly, if responses were "motor" rather than sensory, why should adjacent cells have varied in whether they responded only to visual stimuli, only to tactile stimuli, or to both?
; Kurata et al. 1985; Muakkassa and Strick 1979), might have visual receptive fields that are anchored to the leg or foot, locating stimuli in "foot-centered" coordinates.
have shown that when the monkey's chair is turned, the visual receptive fields of PMv neurons move with the chair. This study demonstrates that the visual receptive fields are not anchored to any external feature of the room, but rather to some part of the monkey's body or of the chair. The result is therefore consistent with our current and previous data showing that most visual receptive fields in PMv are body part centered (see Graziano and Gross 1992; Graziano et al. 1994).
found that the activity of most PMv neurons was modulated by the position of the eyes. However, those authors also suggested that the visual receptive fields in PMv are anchored to the retina and move as the eye moves. Our findings contradict this suggestion. Boussaoud et al. gave three examples of receptive fields that moved with the eye and one example of a receptive field that did not move with the eye. Given the small number of cells those researchers described, it is difficult to compare these proportions with our own results. In any case, as Boussaoud et al. discuss, they do not appear to have tested the visual responses of bimodal, visual-somatosensory neurons. Rather, they tested responses of a subset of neurons associated with the monkey's performance of a lever-press task. Therefore the type of neuron and the type of response studied by Boussaoud et al. are unlikely to be the same as the ones that we studied.
reported them in area PO of the monkey parietal cortex, Pigarev and Rodionova (1986) reported them in the parietal cortex of the cat, and Schlag et al. (1980) reported them in the thalamus of the cat. However, although these visual receptive fields did not move when the eyes moved and therefore were not anchored to the retina, it is not clear what part of the body or world they might have been anchored to. In the crayfish, Weirsma (1966) reported visual receptive fields that were fixed with respect to the gravitational vertical. Visual receptive fields influenced by the direction of gravity have also been reported in striate cortex of the cat (Horn and Hill 1969).
; Millar 1994). Although some of this spatial and visuomotor ability is thought to be present at birth, much of it develops through experience.
; Gross and Graziano 1995). As described above, the body-part-centered visual receptive fields in PMv can encode the distance and direction from a body part to a nearby visual stimulus. Such information is sometimes called "motor error" because it specifies the distance and direction the body part must move to reach or avoid the stimulus (e.g., Bruce 1990). Arm + visual neurons would therefore be useful for guiding the arm toward or away from nearby stimuli. Face + visual neurons would be useful for guiding the head.
in which lesions of PMv disrupted the monkey's ability to avoid or to bite nearby visual stimuli.
recorded from an area on the border of PMv and dorsal premotor cortex and found that each neuron responded best as the monkey reached in a particular direction. That is, the neuron had a motor field. When the arm was moved to a different position, the motor field also moved, rotating roughly with the arm. Therefore the motor fields were arm centered, just as the visual receptive fields in our experiments were arm centered.
analyzed the pattern of errors when human subjects reached toward visual and remembered targets, and concluded that reaching must be controlled in a coordinate system centered roughly on the shoulder. Tipper et al. (1992) found that the attended region of space during a reaching task is anchored to the hand. Paillard (1991) tested human subjects who were wearing displacing prisms. As expected, by repeatedly pointing toward visual targets the subjects were able to adapt to the prisms. Paillard then showed that the movements of each body part, such as the hand, the forearm, the upper arm, and the head, could be separately adapted. All of these experiments suggest that arm movements may be organized in a body-part-centered coordinate frame.
; Duhamel et al. 1992; Groh and Sparks 1996; Mazzoni et al. 1996; Sparks 1991). Thus a general principle of sensory-motor control appears to be that the sensory stimulus is located in a coordinate frame centered on the relevant body part.
; Andersen at al. 1985, 1990) studied the visual responses of neurons in posterior parietal areas 7a and LIP, and found that the visual receptive fields were retinocentric, moving as the eye moved. Those researchers also found that for some cells the magnitude of the visual response was modulated by the position of the eye. [A similar modulation by eye position has since been reported for a number of other visual areas, including PO, area V3a, primary visual cortex, and the lateral geniculate nucleus (Galletti and Battaglini 1989; Galletti et al. 1993; Lal and Friedlander 1989; Trotter et al. 1992)]. Modulation of neuronal activity by the position of the head has now been reported in area 7a and LIP (Andersen et al. 1993; Brotchie et al. 1995). There is even some evidence that neurons in area 7a may be modulated by the position of the arm (MacKay 1992).
; Brotchie et al. 1995; Gross and Graziano 1995; Pouget et al. 1993; Salinas and Abbot 1995). Area 7a and LIP do not project directly to PMv, but they do project to parietal area 7b, which then projects to PMv (Cavada and Goldman-Rakic 1989a,b; Kunzle 1978; Matelli et al. 1986; Mesulam et al. 1977). Proprioceptive input to PMv about head and arm position could also come via projections from other sources, such as the supplementary motor cortex and M1 (e.g., Matelli et al. 1986; Muakkassa and Strick 1979; for review, see Kalaska and Crammond 1992).
,b, 1991; Kunzle 1978; Matelli et al. 1986; Mesulam et al. 1977; Parthasarathy et al. 1992; Weber and Yin 1984). We suggest that these four areas form a bimodal, visual-somesthetic system that processes the space on and near the body, for the purpose of guiding movement.
; Crutcher and Delong 1984a,b; Liles 1985). These somatosensory and motor fields are organized somatotopically. We recorded from the putamen both in anesthetized and awake macaque monkeys (Graziano and Gross 1993, 1995) and found that ~30% of the cells with a somatosensory response on the face or arms also responded to visual stimuli. For these bimodal, visual-tactile neurons, the location of the visual receptive field closely matched the location of the tactile receptive field, extending outward from the skin into the space surrounding the body. In some cases, when the tactile response was on the arm, the visual receptive field was anchored to the arm, moving through space when the arm was moved. Responses in the putamen were somewhat different from the responses that we observed in PMv, in that the tactile and visual receptive fields were usually smaller in the putamen, and therefore the somatotopic map was more clear and had less overlap between the representations of different body parts.
studied neurons in area VIP and found that ~70% were bimodal, responding to tactile stimuli on the face and to visual stimuli near the face. Some cells responded to visual stimuli only within a few centimeters of the tactile receptive field, whereas others responded to more distant stimuli. Most cells were directionally selective in both modalities, and the preferred direction in the tactile modality usually matched the preferred direction in the visual modality. For at least one neuron, the visual response did not change when the eyes moved. This neuron preferred a visual stimulus approaching the chin but not the forehead, regardless of whether the animal's gaze was directed upward or downward.
; Robinson and Burton 1980a,b). About 30% of the neurons in area 7b also respond to visual stimuli; that is, they are bimodal (Hyvarinen 1981; Hyvarinen and Poranen 1974; Leinonen and Nyman 1979; Leinonen et al. 1979). These bimodal neurons have tactile receptive fields on the arm, the face, or both, and visual receptive fields that roughly match the locations of the tactile receptive fields. We recorded from area 7b in anesthetized monkeys (Graziano and Gross 1995; Graziano et al. 1996) and found that for most bimodal cells the tactile and visual receptive fields were bilateral and so large that it was difficult to assess whether the two matched. The visual receptive fields, however, often had a smaller region of best response. When the arm was moved, the region of best visual response did not move with it. Instead, the visual receptive field remained in the same place, unassociated with the arm.
area 7b, VIP, PMv, and the putamenthat contain similar bimodal, visual-somesthetic responses. What, if any, are the differences between these areas? It is difficult to compare VIP with the other areas because it was studied under different conditions. The bimodal properties in the putamen, PMv, and area 7b, however, are not identical. In PMv and the putamen, many of the arm cells had visual receptive fields that were anchored to the arm, moving as the arm was moved; in area 7b, this was never the case. The tactile and visual receptive fields were smallest in the putamen, intermediate in PMv, and largest in area 7b. The somatotopic map was most clear in the putamen, with very little overlap between the representations of different body parts, and was almost undetectible in area 7b. These differences suggest that each bimodal area serves a different function. One speculation is that area 7b forms an early stage in the processing of space near the body, where the information is not as fully processed, perhaps coarse-coded in the form of large receptive fields that are not anchored to specific body parts. The output from area 7b might then be used to help construct the body-part-centered visual receptive fields found in the putamen and PMv.
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ACKNOWLEDGEMENTS |
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We thank G. Yap, H. Biola, D. Evert, N. Rebmann, H. Rodman, D. Prentice, and G. Rizzolatti for help in different phases of the study.
This work was supported by National Eye Institute Grant EY-11347 and McDonnell Pew 90-16.
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FOOTNOTES |
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Address for reprint requests: M. Graziano, Dept. of Psychology, Green Hall, Princeton University, Princeton, NJ 08544.
Received 11 June 1996; accepted in final form 14 January 1997.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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N. R. McFarland and S. N. Haber Convergent Inputs from Thalamic Motor Nuclei and Frontal Cortical Areas to the Dorsal Striatum in the Primate J. Neurosci., May 15, 2000; 20(10): 3798 - 3813. [Abstract] [Full Text] [PDF]
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M. Rijntjes, C. Dettmers, C. Buchel, S. Kiebel, R. S. J. Frackowiak, and C. Weiller A Blueprint for Movement: Functional and Anatomical Representations in the Human Motor System J. Neurosci., September 15, 1999; 19(18): 8043 - 8048. [Abstract] [Full Text] [PDF]
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M. S. A. Graziano Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position PNAS, August 31, 1999; 96(18): 10418 - 10421. [Abstract] [Full Text] [PDF]
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K. Kurata and E. Hoshi Reacquisition Deficits in Prism Adaptation After Muscimol Microinjection Into the Ventral Premotor Cortex of Monkeys J Neurophysiol, April 1, 1999; 81(4): 1927 - 1938. [Abstract] [Full Text] [PDF]
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