Functions of the Basal Ganglia
Motor functions
The function of the basal ganglia in motor control is not understood in detail. It appears that the basal ganglia is involved in the enabling of practiced motor acts and in gating the initiation of voluntary movements by modulating motor programs stored in the motor cortex and elsewhere in the motor hierarchy (Figure 4.6). Thus, voluntary movements are not initiated in the basal ganglia (they are initiated in the cortex); however, proper functioning of the basal ganglia appears to be necessary in order for the motor cortex to relay the appropriate motor commands to the lower levels of the hierarchy.
Recall that the major output from the basal ganglia is an inhibitory connection from the GPint (or SNr) to the thalamus (or superior colliculus). Studies of eye movements in monkeys have shed light on the function of the basal ganglia loop. Normally, the SNr neurons are tonically active, suppressing the output of the collicular neurons that control saccadic eye movements. When the direct pathway striatal neurons are excited by the cortical frontal eye fields, the SNr neurons are momentarily inhibited, releasing the collicular neurons from inhibition. This allows the appropriate collicular neurons to signal the target of the eye movement, allowing the monkey to change its gaze to a new location. The movement was initiated in the frontal eye fields; however, the proper activation of the eye movement required that collicular neurons be released from the inhibition of the basal ganglia.
What is the function of the tonic inhibitory output of the basal ganglia? Recall from the Motor Cortex chapter that stimulating the motor cortex of monkeys at various locations results in stereotyped sequences of movements, such as bringing the hand to the mouth or adopting a defensive posture. It appears that a number of “primitive” motor programs are stored in the cortex, and motor control may require the activation of these elemental motor programs in the precise temporal order to accomplish a sophisticated motor plan. It is important that only one motor program be active at a given time, however, such that one motor act (e.g., use hand to bring food to the mouth) is not competing with a conflicting motor act (e.g., use hand to shield face from dangerous object). It is thought that the basal ganglia is normally active in suppressing inappropriate motor programs, and that activation of the direct pathway temporarily releases one motor program from inhibition, enabling it to be executed by the organism. Thus, the basal ganglia act as a gate that enables the execution of automatic programs in the hierarchy.
Which motor programs should be released from inhibition at a given moment? The basal ganglia may have a major role in learning what motor acts result in rewards for the organism. This information is provided by the dopaminergic neurons of the SNc and ventral tegmental nucleus. Recordings from these neurons in monkeys have shown that they tend to respond when the monkey receives an unexpected reward, and they tend to be inhibited when the monkey fails to receive an expected reward (Figure 4.7). Because the net effect of activation of the nigrostriatal pathway is to excite the direct pathway and inhibit the indirect pathway, this pattern of dopaminergic firing may be involved in tuning the relative balance of direct/indirect pathway activity to enhance the firing of cortical motor programs that produce rewarding outcomes and to suppress the activity of motor programs that do not result in reward. In this way, motor habits can be constructed that tend to reward the animal.
Cognitive functions
As mentioned earlier, there are a number of cortical loops through the basal ganglia that involve prefrontal association cortex and limbic cortex. Through these loops, the basal ganglia are thought to play a role in cognitive function that is similar to their role in motor control. That is, the basal ganglia are involved in selecting and enabling various cognitive, executive, or emotional programs that are stored in these other cortical areas. Moreover, the basal ganglia appear to be involved in certain types of learning. For example, in rodents the striatum is necessary for the animal to learn certain stimulus-response tasks (e.g., make a right turn if stimulus A is present and make a left turn if stimulus B is present). Recordings from rat striatal neurons show that early in training, striatal neurons fire at many locations while a rat learns such a task on a T-shaped maze (Figure 4.8). This suggests that initially the striatum is involved throughout the execution of the task. As the animal learns the task and becomes exceedingly good at its performance, the striatal neurons change their activity patterns, firing only at the beginning of the trial and at the end. It appears that the learned programs to solve this task are now stored elsewhere; the firing of the striatal neurons at the beginning of the maze presumably reflects the enabling of the appropriate motor/cognitive plan in the cortex, and the firing at the end of the maze is presumably involved in evaluating the reward outcome of the trial.
In humans, the basal ganglia appear to be necessary for certain forms of implicit memory tasks. Like motor habit learning discussed above, many types of cognitive learning require repeated trials and are often unconscious. An example is probabilistic classification (Figure 4.9). In this type of task, people have to learn to classify objects based on the probability of belonging to a class, rather than on any explicit rule. In one experiment, subjects were shown a deck of cards with different symbols. Each symbol was associated with a certain probability of predicting rain or sunshine, and the subjects had to say on each trial whether the symbol was a predictor of rain or sunshine. Because the same symbol sometimes predicted sunshine and other times predicted rain, the subjects could not devise a simple rule, and they made many errors at first. Over time, however, they began to get better at classifying the symbols appropriately, although they still often claimed to be guessing. Patients with basal ganglia disorders were impaired at this task, suggesting that the processing of the cognitive loops of the basal ganglia are somehow involved in our ability to subconsciously learn the probabilities of predicted outcomes associated with particular stimuli.
