Cortical populations and behaviour: Hebb's thread.

Abstract This paper discusses work on the function of the motor cortex as revealed by single cell recordings in monkeys and artificial neural network modelling. Our key conceptual approach both in behavioural neuroscience and neural network modeling of motor cortical function relies on reconstructing, visualizing, and modelling the activity in neuronal populations, indeed a key concept advanced by Hebb (1949). The behaviour investigated ranges from exertion of isometric force to pointing movements to complex cognitive processing. The functional properties of single cells with respect to the direction of movement in space are described as well as a population code which provides a unique measure for this direction. Finally, the results of modeling studies are discussed in which directional population activity is used as an input to an artificial neural network to drive a simulated arm. The motor cortex occupies a crucial node in brain control of motor function. It provides major outputs to the spinal cord and brainstem, and is heavily interconnected with other cortical areas as well as the cerebellum and the basal ganglia. The question of how the motor cortex performs its function has been intensely investigated during the past century but it is only during the last 25 years that major advances have been made due to the development of a technique (Ricci et al., 1958) by which the ongoing activity of cells in the motor cortex could be recorded in awake, behaving animals (Evans, 1968). Several studies showed that changes in motor cortical cell activity precedes the development of the motor output and relates quantitatively to its intensity and spatial characteristics (for reviews, see Evans, 1981; Georgopoulos, 1990). Specifically, when reaching in space, cell activity during the reaction time relates primarily to the direction of the movement and less to its extent (Fu et al., 1995; Georgopoulos, 1990). Under isometric conditions, when a static force is exerted, cell activity relates to the magnitude (see Evans, 1981) and direction (Kalaska et al., 1989; Taira et al., 1995) of force, and when a force pulse is developed, cell activity relates to the incremental, dynamic force exerted but not to the total force output (Georgopoulos et al., 1992). Directional Tuning of Single Cells A major aspect of the spatial characteristics of the motor output, be it movement or isometric force, is its direction in space. Cells in the motor cortex (Caminiti et al., 1990; Georgopoulos et al., 1982; Georgopoulos et al., 1986; Kalaska et al., 1989; Schwartz, 1992; Schwartz et al., 1988), as well as in other structures (Caminiti et al., 1991; Fortier et al., 1989; Kalaska et al., 1983), are directionally selective and are broadly tuned with respect to the direction of movement. This means that the cell activity is highest for a movement in a particular direction (the cell's preferred direction) and decreases progressively with movements farther and farther away from this direction. The changes in cell activity relate to the direction and not the endpoint of the reaching movement (Georgopoulos et al., 1985). Quantitatively, the crucial variable on which cell activity depends is the angle formed between the direction of the movement and the cell's preferred direction: the intensity of cell activity is a linear function of the cosine of this angle (Georgopoulos et al., 1982; Schwartz et al., 1988). An example is shown in Figure 1. The preferred directions of single cells range throughout the 3-D directional continuum (Schwartz et al., 1988). Directional Coding by Neuronal Populations The broad directional tuning indicates that a given cell participates in movements of various directions, and that a movement in a particular direction will involve the activation of a whole population of cells. Given that single cells are directionally tuned, we proposed a vectorial neural code for the direction of reaching by the neuronal ensemble (Georgopoulos et al. …