Publications

2013

Graziano, M. S. (2013). Consciousness and the Social Brain. Oxford University Press.

2011

Aflalo, ., & Graziano, . (2011). Organization of the macaque extrastriate visual cortex re-examined using the principle of spatial continuity of function. Journal of Neurophysiology, 105(1), 305-320. https://doi.org/10.1152/jn.00795.2010
How is the macaque monkey extrastriate cortex organized? Is vision divisible into separate tasks, such as object recognition and spatial processing, each emphasized in a different anatomical stream? If so, how many streams exist? What are the hierarchical relationships among areas? The present study approached the organization of the extrastriate cortex in a novel manner. A principled relationship exists between cortical function and cortical topography. Similar functions tend to be located near each other, within the constraints of mapping a highly dimensional space of functions onto the two-dimensional space of the cortex. We used this principle to re-examine the functional organization of the extrastriate cortex given current knowledge about its topographic organization. The goal of the study was to obtain a model of the functional relationships among the visual areas, including the number of functional streams into which they are grouped, the pattern of informational overlap among the streams, and the hierarchical relationships among areas. To test each functional description, we mapped it to a model cortex according to the principle of optimal continuity and assessed whether it accurately reconstructed a version of the extrastriate topography. Of the models tested, the one that best reconstructed the topography included four functional streams rather than two, six levels of hierarchy per stream, and a specific pattern of informational overlap among streams and areas. A specific mixture of functions was predicted for each visual area. This description matched findings in the physiological literature, and provided predictions of functional relationships that have yet to be tested physiologically.
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Graziano, M. S., & Kastner, S. (2011). Awareness as a perceptual model of attention. Cognitive Neuroscience, 2(2), 125-127. https://doi.org/10.1080/17588928.2011.585237
We proposed a theory of consciousness in which the machinery for social perception constructs awareness, and awareness is a perceptual model of the process of attention. One can attribute awareness to others or to oneself. Awareness of X is the brain's perceptual metaphor for the deep attentive processing of X. A set of ten comments on our hypothesis are included in this issue. Each comment raises specific points some of which directly challenge the hypothesis. Here we respond to these specific points and challenges.
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Graziano, M. S., & Kastner, S. (2011). Human consciousness and its relationship to social neuroscience: A novel hypothesis. Cognitive Neuroscience, 2(2), 98-113. https://doi.org/10.1080/17588928.2011.565121
A common modern view of consciousness is that it is an emergent property of the brain, perhaps caused by neuronal complexity, and perhaps with no adaptive value. Exactly what emerges, how it emerges, and from what specific neuronal process, is in debate. One possible explanation of consciousness, proposed here, is that it is a construct of the social perceptual machinery. Humans have specialized neuronal machinery that allows us to be socially intelligent. The primary role for this machinery is to construct models of other people's minds thereby gaining some ability to predict the behavior of other individuals. In the present hypothesis, awareness is a perceptual reconstruction of attentional state; and the machinery that computes information about other people's awareness is the same machinery that computes information about our own awareness. The present article brings together a variety of lines of evidence including experiments on the neural basis of social perception, on hemispatial neglect, on the out-of-body experience, on mirror neurons, and on the mechanisms of decision-making, to explore the possibility that awareness is a construct of the social machinery in the brain.
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Graziano, M. S. (2011). Cables vs. networks: old and new views on the function of motor cortex. Journal of Physiology, 589(10), 2439. https://doi.org/10.1113/jphysiol.2011.209767

Early in the physiological study of the motor cortex, one experimental question began to dominate the research. How are points in cortex connected to muscles? The question fosters a simplistic, feed-forward view of motor cortex in which its intrinsic processing is ignored and its function is assumed to be defined almost entirely by the cables that run down to the spinal cord, relay onto motor neurons, and thus cause muscle contraction. This perspective still pervades almost all modern thinking about the motor cortex. As a result, a more realistic view of motor cortex as a control network has been hindered. The study by Capaday et al. (2011), examining the lateral interactions among neurons in motor cortex, represents an important step beyond the limited muscle-map conception and toward a better understanding of the processing network within the cortex itself.

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Graziano, M. S. (2011). New insights into motor cortex. Neuron, 71(3), 387-388. https://doi.org/10.1016/j.neuron.2011.07.014
An exciting new experiment on the motor cortex of monkeys, by Shenoy and colleagues, begins to elucidate how the neuronal ensemble travels in a systematic fashion through state space. This trajectory through state space may help to explain how the motor cortex sets up and then triggers arm movements.
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2010

Graziano, M. S., Ghazanfar, A., & Platt, M. (2010). Ethologically relevant movements mapped on the motor cortex. In Primate Neuroethology (pp. 454-470). Oxford University Press.

Electrical stimulation of the motor cortex of monkeys elicits complex movements that combine many muscles and joints and that resemble fragments of the animal’s normal movement repertoire. Hand-to-mouth movements, reaching movements, defensive movements, and other ethologically relevant actions can be evoked. Different movements are evoked from different locations in motor cortex. The movement repertoire of the monkey appears to be mapped on the cortical sheet in a manner that preserves local continuity. Simple map schemes that have been proposed in the past, such as a map of the body, or a segregation of the motor cortex into separate areas that process different aspects of movement, explain only some aspects of motor cortex organization. More of the subtlety and complexity of the motor cortex topography can be explained by the principle of a highly dimensional movement repertoire that is flattened onto the cortical surface.

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2009

Dombeck, D., Graziano, M., & Tank, D. (2009). Functional clustering of neurons in motor cortex determined by cellular resolution imaging in awake behaving mice. Journal of Neuroscience, 29(44), 13751-13760. https://doi.org/10.1523/JNEUROSCI.2985-09.2009
Macroscopic (millimeter scale) functional clustering is a hallmark characteristic of motor cortex spatial organization in awake behaving mammals; however, almost no information is known about the functional micro-organization (approximately 100 microm scale). Here, we optically recorded intracellular calcium transients of layer 2/3 neurons with cellular resolution over approximately 200-microm-diameter fields in the forelimb motor cortex of mobile, head-restrained mice during two distinct movements (running and grooming). We showed that the temporal correlation between neurons was statistically larger the closer the neurons were to each other. We further explored this correlation by using two separate methods to spatially segment the neurons within each imaging field: K-means clustering and correlations between single neuron activity and mouse movements. The two methods segmented the neurons similarly and led to the conclusion that the origin of the inverse relationship between correlation and distance seen statistically was twofold: clusters of highly temporally correlated neurons were often spatially distinct from one another, and (even when the clusters were spatially intermingled) within the clusters, the more correlated the neurons were to each other, the shorter the distance between them. Our results represent a direct observation of functional clustering within the microcircuitry of the awake mouse motor cortex.
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Macfarlane, N., & Graziano, M. S. (2009). Diversity of grip in Macaca mulatta. Experimental Brain Research, 197(3), 255-268. https://doi.org/10.1007/s00221-009-1909-z
Much of the research on the neuronal basis of prehension focuses on macaque monkeys. Yet most of the behavioral description of grip types pertains to humans and apes. The purpose of the present study was to provide a catalogue and description of basic grip behavior in macaque monkeys. The observational study explored the diversity of grasping behavior in 157 semi-free ranging rhesus macaques. Video footage of monkeys grasping objects ad libitum was analyzed frame-by-frame, and grips were classified based on the skin surface areas that contacted the object. When monkeys held objects for manipulation, 15 distinct grip categories were observed. When monkeys held support points during climbing, two grip categories were observed. Not all grips were performed with the hand. Some involved the mouth, the foot, or an opposition between the forearm and chest. Grip in macaque monkeys is more diverse than the narrow range of grip that is typically studied.
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2008

Aflalo, ., & Graziano, . (2008). Four-dimensional spatial reasoning in humans. Journal of Experimental Psychology, Human Perception and Performance, 34(5), 1066-1077. https://doi.org/10.1037/0096-1523.34.5.1066
Human subjects practiced navigation in a virtual, computer-generated maze that contained 4 spatial dimensions rather than the usual 3. The subjects were able to learn the spatial geometry of the 4-dimensional maze as measured by their ability to perform path integration, a standard test of spatial ability. They were able to travel down a winding corridor to its end and then point back accurately toward the occluded origin. One interpretation is that the brain substrate for spatial navigation is not a built-in map of the 3-dimensional world. Instead it may be better described as a set of general rules for manipulating spatial information that can be applied with practice to a diversity of spatial frameworks.
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Meier, J., Aflalo, T., Kastner, S., & Graziano, M. S. (2008). Complex organization of human primary motor cortex: a high-resolution fMRI study. Journal of Neurophysiology, 100(4), 1800-1812. https://doi.org/10.1152/jn.90531.2008
A traditional view of the human motor cortex is that it contains an overlapping sequence of body part representations from the tongue in a ventral location to the foot in a dorsal location. In this study, high-resolution functional MRI (1.5x1.5x2 mm) was used to examine the somatotopic map in the lateral motor cortex of humans, to determine whether it followed the traditional somatotopic order or whether it contained any violations of that somatotopic order. The arm and hand representation had a complex organization in which the arm was relatively emphasized in two areas: one dorsal and the other ventral to a region that emphasized the fingers. This violation of a traditional somatotopic order suggests that the motor cortex is not merely a map of the body but is topographically shaped by other influences, perhaps including correlations in the use of body parts in the motor repertoire.
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2007

Aflalo, T., & Graziano, M. S. (2007). Relationship between unconstrained arm movements and single-neuron firing in the macaque motor cortex. Journal of Neuroscience, 27(11), 2760-2780. https://doi.org/10.1523/JNEUROSCI.3147-06.2007
The activity of single neurons in the monkey motor cortex was studied during semi-naturalistic, unstructured arm movements made spontaneously by the monkey and measured with a high resolution three-dimensional tracking system. We asked how much of the total neuronal variance could be explained by various models of neuronal tuning to movement. On average, tuning to the speed of the hand accounted for 1% of the total variance in neuronal activity, tuning to the direction of the hand in space accounted for 8%, a more complex model of direction tuning, in which the preferred direction of the neuron rotated with the starting position of the arm, accounted for 13%, tuning to the final position of the hand in Cartesian space accounted for 22%, and tuning to the final multijoint posture of the arm accounted for 36%. One interpretation is that motor cortex neurons are significantly tuned to many control parameters important in the animal's repertoire, but that different control parameters are represented in different proportion, perhaps reflecting their prominence in everyday action. The final posture of a movement is an especially prominent control parameter although not the only one. A common mode of action of the monkey arm is to maintain a relatively stable overall posture while making local adjustments in direction during performance of a task. One speculation is that neurons in motor cortex reflect this pattern in which direction tuning predominates in local regions of space and postural tuning predominates over the larger workspace.
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Graziano, M. S., & Aflalo, T. (2007). Rethinking cortical organization: moving away from discrete areas arranged in hierarchies. The Neuroscientist, 13(2), 138-147. https://doi.org/10.1177/1073858406295918
One way to understand the topography of the cerebral cortex is that "like attracts like." The cortex is organized to maximize nearest neighbor similarity. This principle can explain the separation of the cortex into discrete areas that emphasize different information domains. It can also explain the maps that form within cortical areas. However, because the cortex is two-dimensional, when a parameter space of much higher dimensionality is reduced onto the cortical sheet while optimizing nearest neighbor relationships, the result may lack an obvious global ordering into separate areas. Instead, the topography may consist of partial gradients, fractures, swirls, regions that resemble separate areas in some ways but not others, and in not a lack of topographic maps but an excess of maps overlaid on each other, no one of which seems to be entirely correct. Like a canvas in a gallery of modern art that no two observers interpret the same way, this lack of obvious ordering of high-dimensional spaces onto the cortex might then result in some scientific controversy over the true organization. In this review, the authors suggest that at least some sectors of the cortex do not have a simple global ordering and are better understood as a result of a reduction of a high-dimensional space onto the cortical sheet. The cortical motor system may be an example of this phenomenon. The authors discuss a model of the lateral motor cortex in which a reduction of many parameters onto a simulated cortical sheet results in a complex topographic pattern that matches the actual monkey motor cortex in surprising detail. Some of the ambiguities of topography and areal boundaries that have plagued the attempt to systematize the lateral motor cortex are explained by the model.
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Graziano, M. S., & Aflalo, T. (2007). Mapping behavioral repertoire onto the cortex. Neuron, 56(2), 239-251. https://doi.org/10.1016/j.neuron.2007.09.013
A traditional view of the motor cortex in the primate brain is that it contains a map of the body arranged across the cortical surface. This traditional topographic scheme, however, does not capture the actual pattern of overlaps, fractures, re-representations, and multiple areas separated by fuzzy borders. Here, we suggest that the organization of the motor cortex, premotor cortex, supplementary motor cortex, frontal eye field, and supplementary eye field can in principle be understood as a best-fit rendering of the motor repertoire onto the two-dimensional cortical sheet in a manner that optimizes local continuity.
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2006

Aflalo, T., & Graziano, M. S. (2006). Partial tuning of motor cortex neurons to final posture in a free-moving paradigm. Proceedings of the National Academy of Sciences U. S. A., 103(8), 2909-2914. https://doi.org/10.1073/pnas.0511139103
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.
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Aflalo, T., & Graziano, M. S. (2006). Possible origins of the complex topographic organization of motor cortex: reduction of a multidimensional space onto a two-dimensional array. Journal of Neuroscience, 26(23), 6288-6297. https://doi.org/10.1523/JNEUROSCI.0768-06.2006
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.
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Graziano, M. S., & Latash, . (2006). Feedback remapping and the cortical control of movement. In Motor Control and Learning (pp. 97-104). Springer.
Motor cortex in the primate brain controls movement at a complex level. For example, electrical stimulation of motor cortex on a behavioral time scale can elicit multi-joint movements that resemble common gestures in the monkey’s behavioral repertoire. How is this complex control accomplished? It was once hypothesized that motor cortex contains a topographic, one-to-one map from points in cortex to muscles. It is now well known that the topography contains a considerable degree of overlap and that the mapping between points in cortex and muscles is many-to-many. However, can a fixed, many-to-many map account for the complex manner in which motor cortex appears to control movement? Recent experiments suggest that the mapping between cortex and muscles may be of a higher order than a fixed, many-to-many map; it may continuously change depending on proprioceptive feedback from the limb. This “feedback remapping” may be a fundamental aspect of motor control, allowing motor cortex to flexibly control almost any high-level or low-level aspect of movement.
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Graziano, M. (2006). The organization of behavioral repertoire in motor cortex. Annual Review of Neuroscience, 29, 105-134. https://doi.org/10.1146/annurev.neuro.29.051605.112924
Motor cortex in the primate brain was once thought to contain a simple map of the body's muscles. Recent evidence suggests, however, that it operates at a radically more complex level, coordinating behaviorally useful actions. Specific subregions of motor cortex may emphasize different ethologically relevant categories of behavior, such as interactions between the hand and the mouth, reaching motions, or defensive maneuvers to protect the body surface from impending impact. Single neurons in motor cortex may contribute to these behaviors by means of their broad tuning to idiosyncratic, multijoint actions. The mapping from cortex to muscles is not fixed, as was once thought, but instead is fluid, changing continuously on the basis of feedback in a manner that could support the control of higher-order movement parameters. These findings suggest that the motor cortex participates directly in organizing and controlling the animal's behavioral repertoire.
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Graziano, M. S. (2006). Progress in understanding spatial coordinate systems in the primate brain. Neuron, 51(1), 7-9. https://doi.org/10.1016/j.neuron.2006.06.011
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.
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Graziano, M. S., & Cooke, D. (2006). Parieto-frontal interactions, personal space, and defensive behavior. Neuropsychologia, 44(6), 845-859. https://doi.org/10.1016/j.neuropsychologia.2005.09.009
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.
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2005

Graziano, M. S., Aflalo, T., & Cooke, D. (2005). Arm movements evoked by electrical stimulation in the motor cortex of monkeys. Journal of Neurophysiology, 94(6), 4209-4223. https://doi.org/10.1152/jn.01303.2004
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.
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Graziano, M. S., Taylor, C., Dylan, D., Moore, ., Humphries, ., & Riddoch, . (2005). A map of complex movements in motor cortex of primates. In Action In Attention (pp. 211-232). Psychology Press.

We used electrical microstimulation to study the organization of motor cortex in awake monkeys. Stimulation on a behaviorally relevant time scale (0.5-1 s) evoked coordinated, complex postures that involved many joints. Postures that involved the arm were arranged across cortex to form a map of hand positions around the body. This map encompassed both primary motor and lateral premotor cortex. Primary motor cortex appeared to represent the central part of the workspace, where monkeys most often manipulate objects with their fingers. These findings suggest that primary motor and lateral premotor cortex might not be arranged in a hierarchy, but instead might operate in parallel, serving different behavioral functions in different parts of the workspace. This hypothesis is also consistent with some of the previous data from motor and premotor cortex.

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2004

Cooke, D., & Graziano, M. S. (2004). Super-flinchers and nerves of steel: defensive movements altered by chemical manipulation of a cortical motor area. Neuron, 43(4), 585-593. https://doi.org/10.1016/j.neuron.2004.07.029
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.
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Cooke, D., & Graziano, M. S. (2004). Sensorimotor integration in the precentral gyrus: polysensory neurons and defensive movements. Journal of Neurophysiology, 91(4), 1648-1660. https://doi.org/10.1152/jn.00955.2003
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.
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Graziano, M. S., Gross, C., Taylor, C., Moore, ., Spence, ., & Driver, . (2004). A system of multimodal areas in the primate brain. In Crossmodal Space and Crossmodal Attention (pp. 51-67). Oxford University Press.
In this chapter, we suggest that a set of interconnected areas in the primate brain monitors the location and movement of objects near the body and controls startle, flinch and defensive responses. This hypothesized “defensive” system, shown in Fig. 1 in a side view of the monkey brain, includes the ventral intraparietal area (VIP), parietal area 7b, the polysensory zone (PZ) in the precentral gyrus, and the putamen. These brain areas are monosynaptically interconnected (Cavada & Goldman-Rakic, 1989a,b; Cavada & Goldman-Rakic, 1991; Matelli et al., 1986; Mesulam et al., 1977; Parthasarathy et al., 1992; Weber & Yin, 1984). Of the four areas, PZ is closest to the motor output, sending direct projections to the spinal cord (Dum & Strick, 1991).
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Graziano, M. S., Gross, C., Taylor, C., Moore, ., Calvert, ., Spence, ., & Stein, . (2004). Multisensory neurons for the control of defensive movements. In The Handbook of Multisensory Processes (pp. 443-452). MIT Press.

If a hornet flies toward your face, you might duck, squint, and lift your hand to block it. If the insect touches your hand, you might withdraw your hand, even pulling it behind your back. These defensive movements have a reflexive quality. They are fast and can occur without conscious planning or thought. They are similar in all people (see Figure 1). However, although they seem reflexive, defensive movements are also highly sophisticated. They can be elicited by touch, sight or sound. They involve coordination between different body parts, such as the arm and head. They are spatially specific: the body parts that move and the direction of movement are appropriate for the location of the threat. The movements can be stronger or weaker depending on external context or the internal state of the person. For example, someone whose “nerves are on edge” may give an exaggerated alerting response to an unexpected stimulus. What sensory-motor pathways in the brain coordinate this rich and complex behavior? We suggest that a special set of interconnected areas in the monkey brain monitors the location and movement of objects near the body and controls startle, flinch and defensive responses. This hypothesized “defensive” system, shown in Figure 2, includes the ventral intraparietal area (VIP), parietal area 7b, the polysensory zone (PZ) in the precentral gyrus, and the putamen. These brain areas are monosynaptically interconnected (Cavada and Goldman-Rakic 1989a,b; Cavada and Goldman-Rakic 1991; Kunzle 1978; Matelli et al. 1986; Mesulam et al. 1977; Parthasarathy et al. 1992; Weber and Yin 1984; Luppino et al., 1999). Of the four areas, PZ is closest to the motor output, sending direct projections to the spinal cord (Dum and Strick 1991). Electrical stimulation of PZ evokes defensive movements, such as withdrawal of the hand, squinting and turning of the head, ducking, or lifting the hand as if to defend the side of the head (Graziano, Taylor and Moore 2002).

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Graziano, M. S., Patel, K., & Taylor, C. (2004). Mapping from motor cortex to biceps and triceps altered by elbow angle. Journal of Neurophysiology, 92(1), 395-407. https://doi.org/10.1152/jn.01241.2003
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.
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Graziano, M. S., Cooke, D., Taylor, C., & Moore, T. (2004). Distribution of hand location in monkeys during spontaneous behavior. Experimental Brain Research, 155(1), 30-36. https://doi.org/10.1007/s00221-003-1701-4
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.
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2003

Cooke, D., Taylor, C., Moore, T., & Graziano, M. S. (2003). Complex movements evoked by microstimulation of the ventral intraparietal area. Proceedings of the National Academy of Sciences U. S. A., 100(10), 6163-6168. https://doi.org/10.1073/pnas.1031751100
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.
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Cooke, D., & Graziano, M. S. (2003). Defensive movements evoked by air puff in monkeys. Journal of Neurophysiology, 90(5), 3317-3329. https://doi.org/10.1152/jn.00513.2003
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.
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2002

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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Graziano, M. S., Taylor, C., Moore, T., & Cooke, D. (2002). The cortical control of movement revisited. Neuron, 36(3), 349-362. Referenced from www.sciencedirect.com: The cortical control of movement revisited
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.
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In a News and Views piece (“Stimulating research on Motor Cortex” 2002, 5:714), Strick comments on our recent finding that microstimulation of motor cortex evokes complex, coordinated behavior (1).  A major concern that he raises is that, “one might ask whether electrical stimulation of the cortex is capable of revealing its function.”  We agree that one should always ask such questions about all experimental methods.  However, a large body of recent work, conspicuously not cited in Strick’s piece, successfully probes cortical function using electrical stimulation.  For example, Newsome and colleagues (2) stimulated monkey visual area MT and influenced the monkey’s perceptual decisions about the direction of motion of visual stimuli.  Romo and colleagues (3) stimulated primary somatosensory cortex and influenced the monkey’s perceptual decisions about tactile stimuli. Shadlen and colleagues (4) stimulated the frontal eye fields and influenced the monkey’s target selection.  Many researchers have used electrical stimulation to study functional maps of eye and head movement (5-7).  We took the well-established protocol of stimulating on a behaviorally relevant time scale and applied it to motor cortex.  The stimulation durations that we used are within the range of these previous studies, and the current intensities are within the range used in the oculomotor studies.  As in previous studies, we evoked meaningful behaviors.

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Graziano, M. S., Botvinick, M., Prinz, ., & Hommel, . (2002). How the brain represents the body: Insights from neurophysiology and psychology. In Common Mechanisms in Perception and Action: Attention and Performance XIX (pp. 136-157). Oxford University Press.

To reach for the computer mouse, sit upright in a chair or hold a journal in order to read it, indeed, to do most of the actions that we commonly perform, we rely on a representation of the spatial configuration of the body. How and where in the brain is the body represented and what are the psychological properties of this body schema? In this article we review first the neurophysiology and then the psychology of the body representation. One finding that has emerged from both approaches is that the body representation is not merely a registration of proprioceptive inputs about joint angle. Instead, the brain contains a sophisticated model of the body that is continually updated on the basis of multimodal input including vision, somesthesis and motor feedback. Neurophysiological studies in the monkey brain show that parietal area 5 is a critical node for processing the body’s configuration. Neurons in area 5 combine signals from different modalities in order to represent limb position and movement. Psychological studies show that the body schema is used to cross-reference between different senses, as a basis for spatial cognition and for movement planning.

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Graziano, M. S., Alisharan, S., Hu, X., & Gross, C. (2002). The clothing effect: tactile neurons in the precentral gyrus do not respond to the touch of the familiar primate chair. Proceedings of the National Academy of Sciences U S A, 99(18), 11930-11933. https://doi.org/10.1073/pnas.172380399
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.
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2001

There are currently three main views on the neural basis of visually guided reaching: 1) neurons in the superior parietal lobe guide arm movements in a spatial framework that is centered on the body; 2) neurons in the intraparietal sulcus guide arm movements in a spatial framework that is centered on the eye; 3) neurons in the caudal part of premotor cortex guide arm movements in a spatial framework that is centered on the arm and hand. The three viewpoints are mutually compatible and may fit into a larger pattern. Eye-centered representations of target position, and body-centered representations of arm and hand position, may be integrated to form a hand-centered representation close to the output stage in caudal premotor and primary motor cortex.
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Graziano, M. S. (2001). An awareness of space. Nature, 411, 903-904. Referenced from www.nature.com: An awareness of space

Damage to restricted parts of the brain can cause spatial confusion and even eliminate awareness of large parts of space around the body.  The precise brain areas responsible for spatial awareness, however, are still in debate.

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The primate cerebral cortex has traditionally been divided into separate territories for vision, touch, audition and movement.  These functions are known to overlap in many parts of cortex, but until recently the regions of overlap were not well studied.  In this issue of Neuron, Bremmer et al. report a major advance in understanding at least one set of areas in the human brain in which the senses are integrated.  This finding joins a growing set of work in monkeys and humans on the integration of the senses with each other and with the control of movement.

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2000

Area 5 in the parietal lobe of the primate brain is thought to be involved in monitoring the posture and movement of the body. In this study, neurons in monkey area 5 were found to encode the position of the monkey's arm while it was covered from view. The same neurons also responded to the position of a visible, realistic false arm. The neurons were not sensitive to the sight of unrealistic substitutes for the arm and were able to distinguish a right from a left arm. These neurons appear to combine visual and somatosensory signals in order to monitor the configuration of the limbs. They could form the basis of the complex body schema that we constantly use to adjust posture and guide movement.
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Graziano, ., & Gandhi, . (2000). Location of the polysensory zone in the precentral gyrus of anesthetized monkeys. Experimental Brain Research, 135(2), 259-266. https://doi.org/10.1007/s002210000518
Neurons in the premotor cortex of macaques respond to tactile, visual and auditory stimuli. The distribution of these responses was studied in five anesthetized monkeys. In each monkey, multiunit activity was studied at a grid of locations across the precentral gyrus. A cluster of sites with polysensory responses was found posterior to the genu of the arcuate sulcus. Tactile and visual responses were represented in all five monkeys, while auditory responses were rarer and found in only two monkeys. This polysensory zone (PZ) was located in the caudal part of premotor cortex. It varied in extent among the monkeys. It was mainly ventral to the genu of the arcuate, in the dorsal and caudal part of the ventral premotor cortex (PMv). In some monkeys it extended more dorsally, into the caudal part of dorsal premotor cortex (PMd). Sensory responses were almost never found in the rostral part of PMd. We suggest that the polysensory zone may contribute to the guidance of movement on the basis of tactile, visual and auditory signals.
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Graziano, M. S., Wheeler, M., Gross, C., & Bolhuis, J. (2000). From vision to action: How the primate brain encodes and remembers visuomotor space. In Brain, Perception, Memory: Advances in Cognitive Neuroscience (pp. 7-15). Oxford University Press.

In 1870, Fritsch and Hitzig first studied primary motor cortex in the monkey brain using electrical stimulation, and in 1881, Hermann Munk used lesion methods to localize the primary visual cortex in the occipital lobe (cited in Gross 1998). Only now, more than one hundred years later, has neuroscience begun to identify the neuronal pathways that connect these two areas. We are finally beginning to understand the routes through which vision is transformed into action.

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1999

In primates, prefrontal, inferior temporal, and posterior parietal cortex are important for cognitive function. It is shown that in adult macaques, new neurons are added to these three neocortical association areas, but not to a primary sensory area (striate cortex). The new neurons appeared to originate in the subventricular zone and to migrate through the white matter to the neocortex, where they extended axons. These new neurons, which are continually added in adulthood, may play a role in the functions of association neocortex.
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Graziano, ., Reiss, ., & Gross, C. (1999). A neuronal representation of the location of nearby sounds. Nature, 397(6718), 428-430. https://doi.org/10.1038/17115
Humans can accurately perceive the location of a sound source-not only the direction, but also the distance. Sounds near the head, within ducking or reaching distance, have a special saliency. However, little is known about this perception of auditory distance. The direction to a sound source can be determined by interaural differences, and the mechanisms of direction perception have been studied intensively; but except for studies on echolocation in the bat, little is known about how neurons encode information on auditory distance. Here we describe neurons in the brain of macaque monkeys (Macaca fascicularis) that represent the auditory space surrounding the head, within roughly 30 cm. These neurons, which are located in the ventral premotor cortex, have spatial receptive fields that extend a limited distance outward from the head.
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A central problem in motor control, in the representation of space, and in the perception of body schema is how the brain encodes the relative positions of body parts. According to psychophysical studies, this sense of limb position depends heavily on vision. However, almost nothing is currently known about how the brain uses vision to determine or represent the location of the arm or any other body part. The present experiment shows that the position of the arm is represented in the premotor cortex of the monkey (Macaca fascicularis) brain by means of a convergence of visual cues and proprioceptive cues onto the same neurons. These neurons respond to the felt position of the arm when the arm is covered from view. They also respond in a similar fashion to the seen position of a false arm.
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Nakamura, ., Chung, ., Graziano, ., & Gross, C. (1999). Dynamic representation of eye position in the parieto-occipital sulcus. Journal of Neurophysiology, 81(5), 2374-2385. https://doi.org/10.1152/jn.1999.81.5.2374
Area V6A, on the anterior bank of the parieto-occipital sulcus of the monkey brain, contains neurons sensitive both to visual stimulation and to the position and movement of the eyes. We examined the effects of eye position and eye movement on the activity of V6A neurons in monkeys trained to saccade to and fixate on target locations. Forty-eight percent of the neurons responded during these tasks. The responses were not caused by the visual stimulation of the fixation light because extinguishing the fixation light had no effect. Instead the neurons responded in relation to the position of the eye during fixation. Some neurons preferred a restricted range of eye positions, whereas others had more complex and distributed eye-position fields. None of these eye-related neurons responded before or during saccades. They all responded postsaccadically during fixation on the target location. However, the neurons did not simply encode the static position of the eyes. Instead most (88%) responded best after the eye saccaded into the eye-position field and responded significantly less well when the eye made a saccade that was entirely contained within the eye-position field. Furthermore, for many eye-position cells (45%), the response was greatest immediately after the eye reached the preferred position and was significantly reduced after 500 ms of fixation. Thus these neurons preferentially encoded the initial arrival of the eye into the eye-position field rather than the continued presence or the movement of the eye within the eye-position field. Area V6A therefore contains a representation of the position of the eye in the orbit, but this representation appears to be dynamic, emphasizing the arrival of the eye at a new position.
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1998

Graziano, ., & Gross, C. (1998). Spatial maps for the control of movement. Current Opinion in Neurobiology, 8(2), 195-201. Referenced from www.sciencedirect.com: Spatial maps for the control of movement
Neurons in the ventral premotor cortex of the monkey encode the locations of visual, tactile, auditory and remembered stimuli. Some of these neurons encode the locations of stimuli with respect to the arm, and may be useful for guiding movements of the arm. Others encode the locations of stimuli with respect to the head, and may be useful for guiding movements of the head. We suggest that a general principle of sensory-motor integration is that the space surrounding the body is represented in body-part-centered coordinates. That is, there are multiple coordinate systems used to guide movement, each one attached to a different part of the body. This and other recent evidence from both monkeys and humans suggest that the formation of spatial maps in the brain and the guidance of limb and body movements do not proceed in separate stages but are closely integrated in both the parietal and frontal lobes.
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The ventral premotor cortex (PMv) of the macaque monkey contains neurons that respond both to visual and to tactile stimuli. For almost all of these "bimodal" cells, the visual receptive field is anchored to the tactile receptive field on the head or the arms, and remains stationary when the eyes fixate different locations. This study compared the responses of bimodal PMv neurons to a visual stimulus when the monkey was required to fixate a spot of light and when no fixation was required. Even when the monkey was not fixating and the eyes were moving, the visual receptive fields remained in the same location, near the associated tactile receptive field. For many of the neurons, the response to the visual stimulus was significantly larger when the monkey was not performing the fixation task. In control tests, the presence or absence of the fixation spot itself had little or no effect on the response to the visual stimulus. These results show that even when the monkey's eye position is continuously changing, the neurons in PMv have visual receptive fields that are stable and fixed to the relevant body part. The reduction in response during fixation may reflect a shift of attention from the visual stimulus to the demands of the fixation task.
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1997

Graziano, M. S., Gross, C., Sakata, ., Mikami, ., & Fuster, . (1997). Vision, Movement, and The Monkey Brain. In The Association Cortex: Structure and Function (pp. 219-232). Harwood Academic Publishers.

We find it effortless to reach toward or avoid nearby objects.  However, the spatial and visuo-motor computations must be quite complicated, especially since our eyes, head, limbs, body, and the objects themselves may be continually changing positions. How does the brain construct a representation of the visual space surrounding the body, and how does this representation guide movement?

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