The role of primary motor cortex in goal-directed movements: insights from neurophysiological studies on non-human primates
Introduction
There is little disagreement that primary motor cortex (MI) plays a pivotal role in volitional motor control, such as reaching and grasping objects of interest in the environment. MI receives considerable converging input from many cortical and subcortical regions and it provides the largest contribution to the descending corticospinal tract, with some of these neurons synapsing directly onto α-motoneurons [1]. Many recent reviews have discussed the role of MI in motor control, learning and skill acquisition 2.•, 3., 4.•, 5., 6..
One approach for interpreting brain function is to assess the response characteristics of neurons in awake, behaving animals. These techniques, first developed by H Jasper and applied by E Evarts to the MI of non-human primates [7], provide an important avenue to assess what type of information is represented in the activity patterns of individual neurons. A large body of literature has been generated on the activity of neurons in MI during behavior, but the interpretation of these responses and the associated function of MI remains strongly debated. Here, I discuss aspects of this debate and how it relates to experimental challenges of relating neural activity to specific features of motor performance, as well as the complex role played by MI in controlling motor function.
Section snippets
Population vectors and correlates of hand motion
Neurophysiogical studies conducted in the 70s focused largely on the relationship between the activity of individual neurons in MI and the motor actions at a single-joint. The studies by Georgopoulos and co-workers 8., 9. in the early 80s emphasized the utility of exploring whole-limb reaching movements and examining how the activity across a population of neurons was related to motor behavior. They introduced the population vector method to estimate the relationship between MI activity and the
The relationship between cell activity and motor performance
The fact that the mechanics of the limb influence the activity of neurons in MI is certainly consistent with studies that illustrate that many neurons in this region are sensitive to force output 21., 22., 23. and correlate with proximal-limb electromyographic (EMG) activity 24., 25.. Several mathematical models illustrate how neurons coding either joint kinematics [26] or muscle activities [13] can predict several key properties of neural activity in MI. Yet cells in MI do not appear to
Alternative interpretations for correlations with multiple variables: parallel versus serial representations
Why are there so many different variables reflected in the discharge pattern of neurons in MI? This appears to be a troubling problem within the framework of sensorimotor transformations 40., 41.. This framework is motivated by the fact that goal-directed reaching movements require the brain to convert spatial information on target location initially defined in retinal coordinates into patterns of proximal-arm muscle activity. The expectation is that there must be some and perhaps several
Motor behaviors induced by stimulation in primary motor cortex
The generally accepted view of MI is that it possesses a rather course somatotopic representation, in which a given region of cortex reflects only a small portion of the peripheral motor apparatus 5., 78., 79.. A very different perspective on the role and organization of MI has recently been put forward by Graziano and co-workers 4.•, 80.. They found that microstimulation of MI of non-human primates using high currents (25-150 μA) and long durations (500 ms) evoked complex motor behaviors, such
Conclusions
This review highlights studies on neural activity in MI of non-human primates performing goal-directed limb motor tasks. This work illustrates two key points about this cortical region. First, neural activity in MI does not reflect a single, simple coordinate frame or representation. Rather, neural activity reflects many features of motor performance from high-level goals to low-level details of motor execution. Second, this complex representation of motor action in MI is not surprising when
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
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of special interest
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of outstanding interest
Acknowledgements
SH Scott is supported by a Canadian Institutes of Health Research (CIHR) Investigator salary award, and his research work is supported by grants from CIHR, National Science and Engineering Research Council, and a Premier’s Research Excellence Award. The author would like to thank J Swaine for expert technical support and constructive criticisms on this article from Dr. JF Kalaska.
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