Biomedical subjects
Publications and source records attributed to Michael S A Graziano.
A new study in this issue of Neuron shows that when monkeys reach to a visual target, neurons in the dorsal premotor cortex compare the location of the target, the hand, and the point of visual fixation. The neurons therefore encode space through a combination of eye-centered and hand-centered coordinates.
We propose that some of the features of the topographic organization in motor cortex emerge from a competition among several conflicting mapping requisites. These competing requisites include a somatotopic map of the body, a map of hand location in space, and a partitioning of cortex into regions that emphasize different complex, ethologically relevant movements. No one type of map fully explains the topography; instead, all three influences (and perhaps others untested here) interact to form the topography. A standard algorithm (Kohonen network) was used to generate an artificial motor cortex array that optimized local continuity for these conflicting mapping requisites. The resultant hybrid map contained many features seen in actual motor cortex, including the following: a rough, overlapping somatotopy; a posterior strip in which simpler movements were represented and more somatotopic segregation was observed, and an anterior strip in which more complex, multisegmental movements were represented and the somatotopy was less segregated; a clustering of different complex, multisegmental movements into specific subregions of cortex that resembled the arrangement of subregions found in the monkey; three hand representations arranged on the cortex in a manner similar to the primary motor, dorsal premotor, and ventral premotor hand areas in the monkey; and maps of hand location that approximately matched the maps observed in the monkey.
Motor cortex neurons in the monkey brain were tested with a diverse and naturalistic arm movement set. Over this global set of movements, the neurons showed a limited but significant degree of tuning to the multijoint posture attained by the arm at the end of each movement. Further supporting the hypothesis that the neurons are partially tuned to end posture, the postures preferred by the neurons significantly matched the postures evoked by electrical stimulation of the same cortical sites. However, much of the variance in neuronal activity remained unexplained even by the end-posture model, and thus other variables must have contributed to the response profile of the neurons. One possibility is that motor cortex neurons become tuned to the wide variety of movement parameters that are relevant to the animal's normal behavioral repertoire, and, therefore, any one parameter accounts for only a limited amount of neuronal variance.
In the monkey brain, two interconnected cortical areas have distinctive neuronal responses to visual, tactile, and auditory stimuli. These areas are the ventral intraparietal area (VIP) and a polysensory zone in the precentral gyrus (PZ). The multimodal neurons in these areas typically respond to objects touching, near, or looming toward the body surface. Electrical stimulation of these areas evokes defensive-like withdrawing or blocking movements. These areas have been suggested to participate in a range of functions including navigation by optic flow, attention to nearby space, and the processing of object location for the guidance of movement. We suggest that a major emphasis of these areas is the construction of a margin of safety around the body and the selection and coordination of defensive behavior. In this review, we summarize the physiological properties of these brain areas and discuss a range of behavioral phenomena that might be served by those neuronal properties, including the ducking and blocking reactions that follow startle, the flight zone of animals, the personal space of humans, the nearby, multimodal attentional space that has been studied in humans, the withdrawal reaction to looming visual stimuli, and the avoidance of obstacles during self-motion such as locomotion or reaching.
In the monkey brain, two interconnected cortical areas have distinctive neuronal responses to visual, tactile, and auditory stimuli. These areas are the ventral intraparietal area (VIP) and a polysensory zone in the precentral gyrus (PZ). The multimodal neurons in these areas typically respond to objects touching, near, or looming toward the body surface. Electrical stimulation of these areas evokes defensive-like withdrawing or blocking movements. These areas have been suggested to participate in a range of functions including navigation by optic flow, attention to nearby space, and the processing of object location for the guidance of movement. We suggest that a major emphasis of these areas is the construction of a margin of safety around the body and the selection and coordination of defensive behavior. In this review, we summarize the physiological properties of these brain areas and discuss a range of behavioral phenomena that might be served by those neuronal properties, including the ducking and blocking reactions that follow startle, the flight zone of animals, the personal space of humans, the nearby, multimodal attentional space that has been studied in humans, the withdrawal reaction to looming visual stimuli, and the avoidance of obstacles during self-motion such as locomotion or reaching.
Electrical stimulation of the motor cortex in monkeys can evoke complex, multijoint movements including movements of the arm and hand. In this study, we examined these movements in detail and tested whether they showed adaptability to differing circumstances such as to a weight added to the hand. Electrical microstimulation was applied to motor cortex using pulse trains of 500-ms duration (matching the approximate duration of a reach). Arm movement was measured using a high-resolution three-dimensional tracking system. Movement latencies averaged 80.2 ms. Speed profiles were typically smooth and bell-shaped, and the peak speed covaried with movement distance. Stimulation generally evoked a specific final hand position. The convergence of the hand from disparate starting positions to a narrow range of final positions was statistically significant for every site tested (91/91). When a weight was fixed to the hand, for some stimulation sites (74%), the evoked movement appeared to compensate for the weight in that the hand was lifted to a similar final location. For other stimulation sites (26%), the weight caused a significant reduction in final hand height. For about one-half of the sites (54%), the variation in movement of each joint appeared to compensate for the variation in the other joints in a manner that stabilized the hand in a restricted region of space. These findings suggest that at least some of the stimulation-evoked movements reflect relatively high-level, adaptable motor plans.
In a restricted zone of the monkey motor cortex, neurons respond to objects near, approaching, or touching the body. This polysensory zone was hypothesized to play a role in monitoring nearby stimuli for the guidance of defensive movements. To test this hypothesis, we chemically manipulated sites within that zone by injecting bicuculline (increasing neuronal activity) or muscimol (decreasing neuronal activity). Bicuculline caused the monkey to react in an exaggerated fashion to an air puff on the face and to objects approaching the face, whereas muscimol caused the monkey to react in a reduced fashion. The effects were expressed partly as a motor abnormality (affecting movement of the musculature contralateral to the injection site) but also partly as a sensory enhancement or sensory neglect (affecting responses to stimuli contralateral to the injection site). These findings suggest that the polysensory zone contributes to the ethologically important function of defense of the body.
This experiment used cortical microstimulation to probe the mapping from primary motor cortex to the biceps and triceps muscles of the arm in monkeys. The mapping appeared to change depending on the angle at which the elbow was fixed. For sites in the dorsal part of the arm and hand representation, the effects of stimulation were consistent with initiating a movement of the elbow to an extended angle. Stimulation evoked more triceps activity than biceps activity, and this difference was largest when the elbow was fixed in a flexed angle. For sites in the ventral part of the arm and hand representation, stimulation had the opposite effect, consistent with initiating a movement of the elbow to a flexed angle. For these sites, stimulation evoked more biceps activity than triceps activity, and the difference was largest when the elbow was fixed in an extended angle. For sites located in intermediate positions, stimulation evoked an intermediate effect consistent with initiating a movement of the elbow to a middle, partially flexed angle. For these sites, when the elbow was fixed at a flexed angle, the evoked activity was largest in the triceps, and when the elbow was fixed at an extended angle, the evoked activity was largest in the biceps. These effects were obtained with 400-ms-long trains of biphasic pulses presented at 200 Hz and 30 microA. They were also obtained by averaging the effects of individual, 30-microA pulses presented at 15 Hz. How this stimulation-evoked topography relates to the normal function of motor cortex is not yet clear. One hypothesis is that these results reflect a cortical map of desired joint angle.
Recently it was shown that electrical stimulation of the precentral gyrus of monkeys can evoke complex, coordinated movements. In the forelimb representation, stimulation of each site caused the arm to move to a specific final posture, and thus the hand to move to a location in space. Among these stimulation-evoked hand locations, certain regions of the hand's workspace were more represented than others. We hypothesized that a similar non-uniform distribution of hand location should be present during a monkey's spontaneous behavior. The present study examined the distribution of hand location of monkeys in their home cages. This distribution was similar to that found by stimulation of the precentral gyrus. That is, arm postures that were over-represented in spontaneous behavior were also over-represented in the movements evoked by cortical stimulation.
The precentral gyrus of monkeys contains a polysensory zone in which the neurons respond to tactile, visual, and sometimes auditory stimuli. The tactile receptive fields of the polysensory neurons are usually on the face, arms, or upper torso, and the visual and auditory receptive fields are usually confined to the space near the tactile receptive fields, within about 30 cm of the body. Electrical stimulation of this polysensory zone, even in anesthetized animals, evokes a specific set of movements. The movements resemble those typically used to defend the body from objects that are near, approaching, or touching the skin. In the present study, to determine whether the stimulation-evoked movements represent a normal set of defensive movements, we tested whether they include a distinctive, nonsaccadic, centering movement of the eyes that occurs during defensive reactions. We report that this centering movement of the eyes is evoked by stimulation of sites in the polysensory zone. We also recorded the activity of neurons in the polysensory zone while the monkey made defensive reactions to an air puff on the face. The neurons became active during the defensive movement, and the magnitude of this activity was correlated with the magnitude of the defensive reaction. These results support the hypothesis that the polysensory zone in the precentral gyrus contributes to the control of defensive movements. More generally, the results support the view that the precentral gyrus can control movement at the level of complex sensorimotor tasks.
Electrical stimulation of two connected cortical areas in the monkey brain, the ventral intraparietal area (VIP) in the intraparietal sulcus and the polysensory zone (PZ) in the precentral gyrus, evokes a specific set of movements. In one interpretation, these movements correspond to those typically used to defend the body from objects that are near, approaching, or touching the skin. The present study examined the movements evoked by a puff of air aimed at various locations on the face and body of fascicularis monkeys to compare them to the movements evoked by stimulation of VIP and PZ. The air-puff-evoked movements included a movement of the eyes from any initial position toward a central region and a variety of stereotyped facial, shoulder, head, and arm movements. These movements were similar to those reported on stimulation of VIP and PZ. One difference between the air-puff-evoked movements and those evoked by stimulation of VIP and PZ is that the air puff evoked an initial startle response (a bilaterally symmetric spike in muscle activity) followed by a more sustained, lateralized response, specific to the site of the air puff. In contrast, stimulation of VIP and PZ evoked mainly a sustained, lateralized response, specific to the site of the receptive fields of the stimulated neurons. We speculate that VIP and PZ may contribute to the control of defensive movements, but that they may emphasize the more spatially specific reactions that occur after startle.
Most neurons in the ventral intraparietal area (VIP) of the macaque brain respond to both visual and tactile stimuli. The tactile receptive field is usually on the face, and the visual receptive field usually corresponds spatially to the tactile receptive field. In this study, electrical microstimulation of VIP, but not of surrounding tissue, caused a constellation of movements including eye closure, facial grimacing, head withdrawal, elevation of the shoulder, and movements of the hand to the space beside the head or shoulder. A similar set of movements was evoked by an air puff to the monkey's cheek. One interpretation is that VIP contributes to defensive movements triggered by stimuli on or near the head.
Recently, we found that electrical stimulation of motor cortex caused monkeys to make coordinated, complex movements. These evoked movements were arranged across the cortex in a map of spatial locations to which the hand moved. We suggest that some of the subdivisions previously described within primary motor and premotor cortex may represent different types of actions that monkeys tend to make in different regions of space. According to this view, primary and premotor cortex may fit together into a larger map of manual space.
Neurons in a restricted zone in the precentral gyrus of macaque monkeys respond to tactile, visual, and auditory stimuli. The tactile receptive fields of these multimodal cells are usually located on the face, arm, or upper torso. In the present study, in awake monkeys sitting in a primate chair, the neurons responded to a tactile probe touching the skin within the tactile receptive field. However, the same neurons did not respond when the tactile receptive field was touched by the primate chair, to which the monkey was habituated.
Electrical microstimulation was used to study primary motor and premotor cortex in monkeys. Each stimulation train was 500 ms in duration, approximating the time scale of normal reaching and grasping movements and the time scale of the neuronal activity that normally accompanies movement. This stimulation on a behaviorally relevant time scale evoked coordinated, complex postures that involved many joints. For example, stimulation of one site caused the mouth to open and also caused the hand to shape into a grip posture and move to the mouth. Stimulation of this site always drove the joints toward this final posture, regardless of the direction of movement required to reach the posture. Stimulation of other cortical sites evoked different postures. Postures that involved the arm were arranged across cortex to form a map of hand positions around the body. This stimulation-evoked map encompassed both primary motor and the adjacent premotor cortex. We suggest that these regions fit together into a single map of the workspace around the body.
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