Supplementary motor area encodes reward expectancy in eye-movement tasks.

Neural activity signifying the expectation of reward has been found recently in many parts of the brain, including midbrain and cortical structures. These signals can facilitate goal-directed behavior or the learning of new skills based on reinforcements. Here we show that neurons in the supplementary motor area (SMA), an area concerned with movements of the body and limbs, also carry a reward expectancy signal in the postsaccadic period of oculomotor tasks. While the monkeys performed blocks of memory-guided and object-based saccades, the neurons discharged a burst after a approximately 200-ms delay following the target-acquiring saccade in the memory task but often fired concurrently with the target-acquiring saccade in the object task. The hypothesis that this postsaccadic bursting activity reflects the expectation of a reward was tested with a series of manipulations to the memory-guided saccade task. It was found that although the timing of the bursting activity corresponds to a visual feedback stimulus, the visual feedback is not required for the neurons to discharge a burst. Second, blocks of no-reward trials reveal an extinction of the bursting activity as the monkeys come to understand that they would not be rewarded for properly generated saccades. Finally, the delivery of unexpected rewards confirmed that in many of the neurons, the activity is not related to a motor plan to acquire the reward (e.g., licking). Thus we conclude that reward expectancy is represented by the activity of SMA neurons, even in the context of an oculomotor task. These results suggest that the reward expectancy signal is broadcast over a large extent of motor cortex, and may facilitate the learning of new, coordinated behavior between different body parts.

Analysis of the step response of the saccadic feedback: computational models.

We present results of theoretical analysis and computational simulations of two models of the saccadic burst generator: the Scudder model and the Jurgens model. We used the experimental paradigm of prolonged stimulation in monkey superior colliculus (SC) to compare the performance of the two models. We excluded the Scudder model since it was not capable of reproducing the experimentally observed staircase movements. We modified the Jurgens model by replacing the originally proposed feedback integrator with an active reset mechanism by a leaky integrator. With this modification we have shown that the staircase movement elicited by prolonged stimulation in the SC can be modeled as a damped oscillatory step response of this model. Furthermore, to replicate the changes in the kinetic profiles of the staircase movements with increased stimulation we modified the functionality of the model. Our results suggest that prolonged stimulation of the SC dynamically changes the gains and time constant of the saccadic feedback.

Influence of the superior colliculus on the primate blink reflex.

In this study we used microstimulation to investigate the influence of the superior colliculus on the trigeminal blink reflex. We report that stimulation in the intermediate to deep layers of the tectum produced inhibition of reflex blinks at a latency of approximately 26 ms. We considered the hypothesis that the blink inhibition was mediated via the omnipause neurons (OPNs) of the eye movement control system in the brainstem. Our results show that the least effective sites for suppression were in the rostral colliculus. This is inconsistent with the prediction that OPNs should be maximally recruited from the rostral tectum near the "fixation zone." From these points and other considerations, we conclude that the reflex blink suppression from the superior colliculus is not directly mediated by the OPNs or the saccadic eye movement circuits.

Statistical analysis of the information content in the activity of cortical neurons.

We sought to quantify the information in the activity of posterior parietal neurons in behaving Rhesus monkeys. We found several models that were adequate to represent the neurons' response fields. We used a gaussian model to construct a signal/noise ratio, which provided an estimate of the number of distinguishable levels (NDL) of activity within the response field. For the typical neuron, an unbiased ideal observer could reliably discriminate 3.4 levels of activity. At change levels of detectability, the threshold limit of reliable discrimination, there was an average of 5.8 NDL. We then used the NDL to divide the response field into regions of spatial ambiguity. For an individual neuron, we suggest that firing rate is a measure of the probability that the target is at the center of the neuron's response field.

Analysis of the step response of the saccadic feedback: system behavior.

We used prolonged stimulation of the monkey superior colliculus to elicit staircase eye movements. By changing the parameters of the stimulating current we were able to obtain movements with different dynamics. An increase in the current frequency resulted in the shortening of the intersaccadic interval and a decrease of the amplitudes in the staircase. In cases of high stimulation, after an initial saccade of fixed metrics, the eyes moved in an apparently smooth fashion. The movement was conjugate and in the same direction as the first saccade. By analyzing the velocity trace we found that the movement consisted of a chain of small saccades, each of which started before the previous one ended. We conducted a quantitative analysis of the staircase movements including the cases of apparently smooth movement of the eyes. We conclude that all of the movements elicited by prolonged SC stimulation were generated by the saccadic feedback circuitry. The dynamic profiles of the elicited movements changed continuously with the stimulating current parameters. On one end of the continuum we observed the classically, described staircase movements with individual movements separated in time. On the other end of the continuum we saw the apparent smooth movement as the limit case produced by high stimulation of the SC.