Partial tuning of motor cortex neurons to final posture in a free-moving paradigm

Abstract

Motor cortex neurons in the monkey brain were tested with a diverse and naturalistic arm movement set. Over this global set of movements, the neurons showed a limited but significant degree of tuning to the multijoint posture attained by the arm at the end of each movement. Further supporting the hypothesis that the neurons are partially tuned to end posture, the postures preferred by the neurons significantly matched the postures evoked by electrical stimulation of the same cortical sites. However, much of the variance in neuronal activity remained unexplained even by the end-posture model, and thus other variables must have contributed to the response profile of the neurons. One possibility is that motor cortex neurons become tuned to the wide variety of movement parameters that are relevant to the animal's normal behavioral repertoire, and, therefore, any one parameter accounts for only a limited amount of neuronal variance.

Fig. 1.

Example of a motor cortex neuron that is locally but not globally direction tuned. (A) Front view of 683 hand movements made during 15 min. Each trail of dots represents one movement measured at 14.3-ms intervals. The monkey drawing shows the approximate scale and location of the animal. (B) Firing rate of the neuron during each movement vs. angular deviation (Δθ) between movement vector and preferred vector. Fit line is cosine fit. R² = 0.03; P > 0.05. (C) Seventy-three selected movements that originated within a 5-cm radius sphere and were between 6 and 15 cm in length. (D) Direction tuning over the limited movement set. R² = 0.40; P < 0.0001.

Fig. 2.

Group data comparing different models of neuronal tuning. (A) Direction tuning on a complete movement set (global) resulted in low R² values for most neurons; direction tuning on a limited movement set (local) resulted in significantly higher R² values (ANOVA, F = 192.00, P < 0.0001). (B) Comparison of four models tested on the complete movement set. The four distributions of R² values are significantly different (ANOVA, F = 63.71, P < 0.0001). (C) Same four models as in B but applied to randomized data. The four distributions of R² values are not significantly different (F = 0.92; P = 0.43).

Fig. 3.

Comparison of neuronal tuning and stimulation-evoked postures. (A) Data from an example neuron. The preferred final posture was determined by regression analysis. The final posture of each movement was compared to the preferred posture. The distance between them was calculated in 8D posture space. Distance was measured in units of standard deviations of the Gaussian tuning function to express all eight dimensions in posture space in equivalent units. This distance is plotted on the x axis, and firing rate during the movement is plotted on the y axis. The data fit the Gaussian tuning function with an R² value of 0.38 (P < 0.0001). Electrical stimulation of the same cortical site evoked a final posture. The mean stimulation-evoked posture is plotted (red vertical line) and was near the preferred posture of the neuron. The mean stimulation-evoked postures from other cortical sites (black vertical bars) were farther from the preferred posture of this neuron. (B) For each neuron a percentile was computed indicating how closely the neuron’s preferred posture matched the posture evoked by stimulation of the same cortical site as compared to stimulation of other cortical sites. This distribution is not uniform; it is significantly greater than 50% (binomial test, P < 0.0001).