Specificity of sensorimotor learning and the neural code: Neuronal representations in the primary motor cortex
Introduction
During performance of visually guided movements, the brain transforms visuospatial information into appropriate motor commands [6], [28], [68]. Psychophysical studies suggest that when humans learn a novel visuomotor transformation, an internal model of limb dynamics and kinematics is modified. These internal models allow the motor system to achieve the desired outcome—reaching towards a visible goal—under the new conditions [30], [33], [65], [80]. Learning a new motor skill that requires adaptation to directional errors generalizes poorly across movement directions [16], [32], workspace [19] and posture [3]. This is similar to sensory systems [1], [20], where practice can induce behavioral improvement that is specific to the situation experienced during the practice sessions. These findings suggest a reliance on neuronal elements with localized spatial fields [13], [19], [20]; namely that changes occur in neurons with fine selectivity (i.e., receptive fields, tuning curves) for the stimuli experienced or the movements made during training.
Neuronal elements with selectivity to movement direction are common in many parts of the motor system, including the primary motor cortex (M1) where the majority of cells show directional tuning [17], [26]. M1 participates in the planning and execution of reaching movements [28], [59] and has been shown to be involved in motor learning on the cellular level [51], in human studies [25], [29], [38], [64], and in electrophysiological studies [21], [35], [43], [79]. Only recently, however, an electrophysiological study of M1 linked neuronal selectivity to movement direction with the limited transfer of learning [46].
Although many studies indicate that learning can induce specific changes in brain activity [20], [53], [71], [72], this finding does not necessarily imply that newly learned skills are “better” represented in the brain. The crucial question is: Do neurons encode task parameters, such as movement direction, any better after learning? In the motor system, such improved encoding [9] can be used for decoding by downstream areas and as an efference copy for further computation [69], [80]. It can also be used by an external observer to allow for more accurate prediction of behavior [34], [73]. In a recent study [45], we examined two questions. First, do learning-induced changes in firing rates provide more information on the task? Second, what aspect of cell activity contributes the most to this improvement?
To address the first question, we employed an information-theory analysis [10], [50] to calculate the mutual information (Fig. 7) between cell activity and direction of movement. Informational measures have two relevant advantages. First, they use the full distribution (estimated from the data) of neuronal activity and do not assume any specific shape of the tuning curve or noise distribution. This allows for a more fine-tuned examination of learning-related changes. Second, they provide a measure as to how well different directions can be differentiated, based on neuronal activity. To address the second question, we examined two features of the neuronal response that could contribute to the increase in information: response variability and the slope of the tuning curve. Finally, to demonstrate that the observed increase in information can be extracted, we used the neuronal activity to decode the actual movement direction.
Section snippets
Behavioral paradigm
Monkeys moved a manipulandum to control the movement of a cursor on a video screen located 50 cm from their torso and eyes with the goal of moving the cursor from a starting point at the center of the screen (origin) to a visual target in a delayed go-signal paradigm (Fig. 1a); this required the monkey to hold (as verified by hand velocity and EMG) the cursor in the origin circle for a random 750–1500 ms after the target onset. The disappearance of the origin indicated the go-signal. In each
Results
This report combines and discusses findings described in two recent publications [45], [46].
Discussion and conclusions
The present findings demonstrate a modification in the activity and spatial tuning functions of neurons in the primary motor cortex as a result of learning a local visuomotor skill. We suggest that this altered activity reflects learning and retention of the newly acquired internal model, one that converts visuospatial cues into the motor commands required for hand movements and/or joint rotations to achieve the goal. In addition, we show that these changes affect the efficiency of the neural
Acknowledgements
We thank Chen Nathan and Thomas Boraud for participating in the recordings, Gal Chechick and Amir Globerson for helpful discussions of Information theory and Hagai Bergman and Steven P. Wise for constant help and many fruitful discussions. This study was supported in part by a Center for Excellence grant (8006/00) administered by the ISF, by a BMBF-DIP grant and by grant 2001073 administered by the BSF. We are also thankful for the contributions by the Golden charitable trust and by Avraham and
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