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ScienceWeek
NEUROBIOLOGY: ON THE OUTPUT OF THE MOTOR CORTEX
The following points are made by Marc H. Schieber (Current Biology 2004 14:R353):
1) The mammalian cerebral cortex is arguably the most sophisticated piece of neurobiological information-processing machinery in the brain. Our ability to understand the neural processing accomplished by the cerebral cortex is hampered by the fact that the cortex receives no direct inputs from sensory afferents and has no direct output to muscles. The cortical output that most directly controls bodily movement arises from neurons in layer V of a specialized region, the primary motor cortex (M1). For 140 years, electrical stimulation has been used to investigate the mechanisms through which these motor cortex neurons control muscle contractions and movements. But until now technical obstacles have meant it has not been possible to examine the basic output effects of stimulating a single neuron in the mammalian motor cortex. These obstacles have recently been surmounted by Brecht and colleagues [1], who have reported that intracellular electrical stimulation of single neurons in the motor cortex of intact rats evokes observable whisker movement.
2) Ever since the 1860s, when Gustav Fritsch (1838-1927) and Eduard Hitzig (1838-1907) evoked movements by electrically stimulating the cortex of a dog, researchers have sought to understand the basic units of cortical motor output [2]. Through much of the 20th century, neuroscientists have investigated the effects of stimulating the cortical surface with second-long bursts of alternating current that directly activated many cubic millimeters of cortex and elicited overt movements [3,4]. Later, intracortical microelectrodes were used to deliver millisecond trains of microsecond, microampere current pulses that directly activated only dozens of cortical neurons and evoked brief twitch-like movements [5]. Observations of the movements or muscle contractions evoked by these stimuli led to a long-running debate as to whether the basic unit of cortical output more directly represents muscle contractions or more abstractly represents the movements per se.
3) Extracellular recording from single neurons in awake, behaving animals expanded the possibilities even further. The discharge rate of M1 neurons was found to correlate with a variety of kinematic and dynamic movement parameters, including force, direction, position and velocity. Recent studies have found representations of external target location, or even the ordinal sequence of target appearance in the discharge of motor cortex neurons. What motor output would be observed if one could stimulate a single cortical neuron?
4) Making this observation has been precluded by a "Catch 22": the stable electrical contact needed to stimulate a single cortical neuron can be obtained only under anesthesia, but under anesthesia the spontaneous activity of the nervous system generally is so suppressed that action potentials from a single cortical neuron fail to produce any observable movement. Brecht et al.[1] chose to study a system that circumvented this conundrum. In rats, whisker movements can "escape" spontaneously from sleep paralysis or anesthesia, and hence are suppressed less than other somatic movements. Furthermore, using magnified video monitoring, the researchers were able to track movement of the whiskers with 0.05 deg precision. This combination of nature and technique enabled Brecht et al.[1] to observe whisker movements evoked by intracellular, nanoampere stimulation of single M1 neurons in intact animals. Although the movements evoked were tiny (1 deg), the observations have provided insights into the basic output of the mammalian motor cortex.
References (abridged):
1 Brecht, M., Schneider, M., Sakmann, B., and Margrie, T.W. (2004). Whisker movements evoked by stimulation of single pyramidal cells in rat motor cortex. Nature 427, 704-710
2 Schieber, M.H. (2001). Constraints on somatotopic organization in the primary motor cortex. J. Neurophysiol. 86, 2125-2143
3 Penfield, W. and Boldrey, E. (1937). Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 37, 389-443
4 Woolsey, C.N., Settlage, P.H., Meyer, D.R., Sencer, W., Hamuy, T.P., and Travis, A.M. (1952). Patterns of localization in precentral and "supplementary" motor areas and their relation to the concept of a premotor area. Res. Pub. Assoc. Res. Nerv. Ment. Dis. 30, 238-264
5 Asanuma, H. and Rosen, I. (1972). Topographical organization of cortical efferent zones projecting to distal forelimb muscles in the monkey. Exp. Brain Res. 14, 243-256
Current Biology http://www.current-biology.com
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NEUROBIOLOGY: ON THE CORTICAL MOTOR SYSTEM
The following points are made by M. Alessandra Umilta (Current Biology 2004 14:R204):
1) In a series of experiments in the late 19th century, Gustav Fritsch (1838-1927) and Eduard Hitzig (1838-1907) pioneered the technique of passing an electric current through an electrode placed on the cortical surface of the brain to induce. This has proved to be a powerful tool for studying the functional organization of the frontal cortex, the site of cortical motor control and generation [1]. More recent studies have shown that prolonged intracortical electrical microstimulation in the frontal cortex can evoke complex movements involving different joints and muscles, while short stimulation evokes only simple movements. Short duration stimulation was thought to reduce the spread of current to neighboring cortical regions, providing a more specific stimulus and for this reason a short train of electrical stimulation (10-50 milliseconds) became the technique of choice for studying the frontal cortex [2].
2) In recent years, Researchers [3] have applied long durations of electrical stimulation (up to 500 milliseconds) with some surprising results. Long-duration stimulations were selected in an attempt to match the temporal durations of spontaneous behaviors. These long duration stimulations evoke complex movements, strikingly similar to meaningful behaviors of monkeys. In a recent study, Graziano et al [4] both electrically stimulated and recorded from neurons in the posterior part of the portion of the ventral premotor cortex called F4 [5]. The authors suggest that the posterior half of F4 is a functionally distinct region that they term the "polysensory zone".
3) Previous studies have shown that most F4 neurons respond to tactile stimuli on a particular body part, and some also respond to visual and auditory stimuli. The visual receptive field of such a neuron is located around the part of the body that the neuron responds to during touch, typically extending about 30 centimeters from the body part. Importantly, the visual receptive field is anchored to this particular body part and consequently independent of eye position. Across the population of neurons in this region, the receptive fields are mostly located on the face, shoulder, arm and torso. In addition, most of these neurons discharge with movement of the specific body part. Short duration intracortical microstimulation in this area has demonstrated that these neurons can generate movement of the neck, proximal arm, trunk, face and mouth.
4) The novelty of the new experiments [4] is that long duration (500 millisecond) electrical stimulation was used at relatively high current intensity (usually 20-50 mA and in some cases up to 300 mA). Unlike with a brief stimulation, this evoked coordinated and complex face and eye movements that involved many different muscles. These movements were evoked when the animal was awake and also when the animal was under anaesthesia, ruling out the possibility that they were simply a reaction to a sensory experience. The movements resembled defensive type movements of the kind that can be elicited behaviorally in the same animals by applying an air puff on to the monkey's face.
5) In summary: Prolonged electrical stimulation of the ventral premotor cortex can evoke complex defensive movements. Moreover, neurons in this region exhibit activity correlated with the vigor of an induced defensive reaction. These results support the idea that this cortical region encodes goal-related actions.
References (abridged):
1. Porter, R. and Lemon, R. (1993). Corticospinal function and voluntary movements. (Oxford: Clarendon Press)
2. Tehovnik, E.J. (1996). Electrical stimulation of neural tissue to evoke behavioral responses. J. Neurosci. Meth. 65, 1-17
3. Cooke, D.F. and Graziano, M.S. (2003). Sensorimotor integration in the precentral gyrus: polysensory neurons and defensive movements. J.Neurophysiol (in press)
4. Graziano, M.S., Taylor, C.S., Moore, T., and Cooke, D.F. (2003). The cortical control of movement revisited. Neuron 36, 349-362
5. Matelli, M., Luppino, G., and Rizzolatti, G. (1985). Patterns of cytochrome oxidase activity in the frontal agranular cortex of macaque monkey. Behav. Brain Res. 18, 125-137
Current Biology http://www.current-biology.com
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CODING OF PERIPERSONAL SPACE IN INFERIOR PREMOTOR CORTEX (AREA F4).
The following points are made by L. Fogassi et al (J. Neurophysiol 1996 76:141):
1) The authors report they studied the functional properties of neurons in the caudal part of inferior area 6 (area F4) in awake monkeys. In agreement with previous reports, the large majority (87%) of neurons responded to sensory stimuli. The responsive neurons fell into three categories: somatosensory neurons (30%); visual neurons (14%); and bimodal, visual and somatosensory neurons (56%).
2) Both somatosensory and bimodal neurons typically responded to light touch of the skin. Their receptive fields (RFs) were located on the face, neck, trunk, and arms. Approaching objects were the most effective visual stimuli. Visual RFs were mostly located in the space near the monkey (peripersonal space). Typically they extended in the space adjacent to the tactile RFs.
The coordinate system in which visual RFs were coded was studied in 110 neurons. In 94 neurons the RF location was independent of eye position, remaining in the same position in the peripersonal space regardless of eye deviation. The RF location with respect to the monkey was not modified by changing monkey position in the recording room. In 10 neurons the RF's location followed the eye movements, remaining in the same retinal position (retinocentric RFs). For the remaining six neurons the RF organization was not clear.
The authors refer to F4 neurons with RF independent of eye position as "somatocentered neurons". In most somatocentered neurons (43 of 60 neurons) the background level of activity and the response to visual stimuli were not modified by changes in eye position, whereas they were modulated in the remaining 17.
The authors suggest it is important to note that eye deviations were constantly accompanied by a synergic increase of the activity of the ipsilateral neck muscles. It is not clear, therefore, whether the modulation of neuron discharge depended on eye position or was a consequence of changes in neck muscle activity. The effect of stimulus velocity (20-80 cm/s) on neuron response intensity and RF extent in depth was studied in 34 somatocentered neurons. The results demonstrated that in most neurons the increase of stimulus velocity produced an expansion in depth of the RF.
The authors conclude that space is coded differently in areas that control somatic and eye movements. The authors suggest that space coding in different cortical areas depends on the computational necessity of the effectors they control.
Journal of Neurophysiology http://jn.physiology.org
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