As monkeys perform schedules containing several trials with a visual cue indicating reward proximity, their error rates decrease as the number of remaining trials decreases, suggesting that their motivation and/or reward expectancy increases as the reward approaches. About one-third of single neurons recorded in the anterior cingulate cortex of monkeys during these reward schedules had responses that progressively changed strength with reward expectancy, an effect that disappeared when the cue was random. Alterations of this progression could be the basis for the changes from normal that are reported in anterior cingulate population activity for obsessive-compulsive disorder and drug abuse, conditions characterized by disturbances in reward expectancy.

Many lines of evidence suggest that the cerebellum is involved in motor control. But what features of these movements are encoded by cerebellar neurons? For slow-tracking eye movements, the activity of Purkinje cells in the ventral paraflocculus of the cerebellum is known to be correlated with eye velocity and acceleration. Here we show that the complex temporal pattern of the firing frequency that occurs during the ocular following response elicited by movements of a large visual scene can be reconstructed by an inverse-dynamics representation, which uses the position, velocity and acceleration of eye movements. Further analysis reveals that the velocity and acceleration components can provide appropriate dynamic drive signals to ocular motor neurons, whereas the position component often has the wrong polarity. We conclude that these Purkinje cells primarily contribute dynamic command signals.

1. We studied response properties of neurons in the superior temporal sulcus (STS) of behaving monkeys that discharged during brief, sudden movements of a large-field visual stimulus, eliciting ocular following. Most neurons responded to movements of a large-field visual stimulus with directional selectivity, preferring high stimulus speeds. Neurons were mostly recorded in the medial superior temporal area (MST) (187/250) and the middle temporal area (MT) (57/250). Further response properties were studied in the MST neurons. 2. Response latencies were measured when a large-field random dot pattern was moved in the preferred direction and preferred speed for each neuron. Eighty percent (120/150) of the neurons were activated < 50 ms after the onset of the stimulus motion. In most cases (89%, 134/150), increased firing rates started before the eye movements, with 59% (88/150) starting > 10 ms before the eye movements. 3. The relationship between the latency of neuronal responses and that of eye movements was studied in 59 neurons by changing the stimulus speed systematically (10-160 degrees/s). The latencies of both neuronal and ocular responses decreased as stimulus speed increased. As a result, the time difference between the response latencies for neuronal and ocular responses varied little with changes in stimulus speed. 4. Blurring of the random dot pattern, by interposing a sheet of ground glass, increased the latency of both neuronal responses and eye movements. 5. With the use of a check pattern instead of random dots, both neuronal and ocular responses began to decrease rapidly when the temporal frequency of the visual stimulus exceeded 20 Hz. At 40 Hz the neurons showed a distinctive burst-and-pause firing pattern, and the eye movements showed signs of oscillation. 6. The response properties of the MST neurons during ocular following were similar to those of the dorsolateral pontine nucleus (DLPN) neurons, reported previously. Our results indicate that the MST neurons may provide visual information to the DLPN neurons and may play a role in eliciting ocular following. 7. Responses during smooth-pursuit eye movement were studied in 55 MST neurons. Each of these neurons responded to the moving large-field visual stimulus, which elicited ocular following, and 40 of these neurons were activated during smooth pursuit in the dark. Response latencies during smooth pursuit were long in those neurons having different directional preferences during smooth pursuit and ocular following but were short for those having the same directional preferences during smooth pursuit and ocular following.(ABSTRACT TRUNCATED AT 400 WORDS)

Single neurons in the ventral striatum of primates carry signals that are related to reward and motivation. When monkeys performed a task requiring one to three bar release trials to be completed successfully before a reward was given, they seemed more motivated as the rewarded trials approached; they responded more quickly and accurately. When the monkeys were cued as to the progress of the schedule, 89 out of 150 ventral striatal neurons responded in at least one part of the task: (1) at the onset of the visual cue, (2) near the time of bar release, and/or (3) near the time of reward delivery. When the cue signaled progress through the schedule, the neuronal activity was related to the progress through the schedule. For example, one large group of these neurons responded in the first trial of every schedule, another large group responded in trials other than the first of a schedule, and a third large group responded in the first trial of schedules longer than one. Thus, these neurons coded the state of the cue, i.e., the neurons carried the information about how the monkey was progressing through the task. The differential activity disappeared on the first trial after randomizing the relation of the cue to the schedule. Considering the anatomical loop structure that includes ventral striatum and prefrontal cortex, we suggest that the ventral striatum might be part of a circuit that supports keeping track of progress through learned behavioral sequences that, when successfully completed, lead to reward.

The simple-spike firing frequency of 30 Purkinje cells (P cells) in the ventral paraflocculus (VPFL) of alert monkeys was studied in relation to vertical slow eye movements, termed ocular following response (OFR), induced by large-field visual motions of different velocities and durations. To quantitatively analyze the relationship between eye movement and firing frequency, an inverse dynamics representation of the eye movement was used for reconstructing the temporal waveform of firing. Coefficients of eye-acceleration, velocity, and position, bias, and time lag between firing and eye movement were estimated by least-square error method. In the regression analyses for each stimulus condition, 86% (146/170) of the well-modulated temporal firing patterns taken from those 30 P cells were reconstructed successfully from eye movement. The model with acceleration, velocity, and position terms, which we used, was shown as the best among several potential models by Cp statistics, consistent with t-test of significance of each term. Reliable coefficients were obtained from 75% (109/146) of the well-reconstructed firing patterns of 28 cells among 30. The estimated coefficients were larger (statistically significant) for slow stimuli than for fast stimuli, suggesting changes in sensitivities under different conditions. However, firing patterns of each cell under several different conditions were frequently well reconstructed by an inverse dynamics representation with a single set of coefficients (13 cells among 21). This indicates that the relationships between P cell firing and OFR are roughly linear in those stimulus ranges. The estimated coefficients for acceleration and velocity suggested that the VPFL P cells properly encode the dynamic components of the motor command during vertical OFR. As for the positional component, however, these P cells are correlated with eye movement in the opposite direction. In the regression analysis without positional component, remarkable differences between observed and reconstructed firing patterns were noted especially in the initial phase of the movements, indicating that the negative positional component was not negligible during OFR. Thus we conclude that, during OFR, the VPFL P cells cannot provide the necessary final motor command, and other brain regions, downstream neural structures, or other types of P cells must provide lacking position-dependent motor commands. This finding about the negative correlation with the position is in the opposite sign with previous studies obtained from the fixation and the smooth pursuit movement. From these comparisons, how the VPFL contributes to a part of the final motor command or how other brain regions complement the VPFL is suggested to be different for early and late phases of the movements.