Churchland, M. M., Cunningham, J. P., Kaufman, M. T., Ryu, S. I., and Shenoy, K. V.

Neuron, 68:387 – 400, *2010*

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### Abstract

Summary The motor cortices are active during both movement and movement preparation. A common assumption is that preparatory activity constitutes a subthreshold form of movement activity: a neuron active during rightward movements becomes modestly active during preparation of a rightward movement. We asked whether this pattern of activity is, in fact, observed. We found that it was not: at the level of a single neuron, preparatory tuning was weakly correlated with movement-period tuning. Yet, somewhat paradoxically, preparatory tuning could be captured by a preferred direction in an abstract #space# that described the population-level pattern of movement activity. In fact, this relationship accounted for preparatory responses better than did traditional tuning models. These results are expected if preparatory activity provides the initial state of a dynamical system whose evolution produces movement activity. Our results thus suggest that preparatory activity may not represent specific factors, and may instead play a more mechanistic role.

### Review

What are the variables that best explain the preparatory tuning of neurons in dorsal premotor and primary motor cortex of monkeys doing a reaching task? This is the core question of the paper which is motivated by the observation of the authors that preparatory and perimovement (ie. within movement) activity of a single neuron may even qualitatively differ considerably (something conflicting with the view that preparatory activity is a subthreshold version of perimovment activity). This observation is experimentally underlined in the paper by showing that average preparatory activity and average perimovement activity of a single neuron are largely uncorrelated for different experimental conditions.

To quantify the suitability of a set of variables to explain perparatory activity of a neuron the authors use a linear regression approach in which the values of these variables for a given experimental condition are used to predict the firing rate of the neuron in that condition. The authors compute the generalisation error of the learnt linear model with crossvalidation and compare the performance of several sets of variables based on this error. The variables performing best are the principal component scores of the perimovement population activity of all recorded neurons. The difference to alternative sets of variables is significant and in particular the wide range of considered variables makes the result convincing (e.g. target position, initial velocity, endpoints and maximum speed, but also principal component scores of EMG activity and kinematic variables, i.e. position, speed and acceleration of the hand). That perimovement activity is the best regressor for preparatory activity is quite odd, or as Burak aptly put it: “They are predicting the past.”

The authors suggest a dynamical systems view as explanation for their results and hypthesise that preparatory activity sets the initial state of the dynamical system constituted by the population of neurons. In this view, the preparatory activity of a single neuron is not sufficient to predict its evolution of activity (note that the correlation between perparatory and perimovement activity assesses only one particular way of predicting perimovement from preparatory activity – scaling), but the evolution of activity of all neurons can be used to determine the preparatory activity of a single neuron under the assumption that the evolution of activity is governed by approximately linear dynamics. If the dynamics is linear, then any state in the future is a linear transformation of the initial state and given enough data points from the future the initial state can be determined by an appropriate linear inversion. The additional PCA, also a linear transformation, doesn’t change that, but makes the regression easier and, important for the noisy data, also regularises.

These findings and suggestions are all quite interesting and certainly fit into our preconceptions about neuronal activity, but are the presented results really surprising? Do people still believe that you can make sense of the activity of isolated neurons in cortex, or isn’t it already accepted that population dynamics is necessary to characterise neuronal responses? For example, Pillow et al. (Pillow2008) used coupled spiking models to successfully predict spike trains directly from stimuli in retinal ganglion cells. On the other hand, Churchland et al. indirectly claim in this paper that the population dynamics is (approximately) linear, which is certainly disputable, but what would nonlinear dynamics mean for their analysis?