We have now reached the top of the cognitive neuroscience hierarchy: the "executive" level. In a business, an executive makes important decisions and plans, based on high-level information coming in from all the different divisions of the company, and with a strong consideration of "the bottom line." In a person, the executive level of processing, thought to occur primarily within the prefrontal cortex (PFC), similarly receives high-level information from posterior cortical association areas, and is also directly interconnected with motivational and emotional areas that convey "the bottom line" forces that ultimately guide behavior. Although many of us walk around with the impression (delusion?) that our actions are based on rational thought and planning, instead it is highly likely that basic biological motivations and affective signals play a critical role in shaping what we do. At least, this is what the underlying biology of the PFC and associated brain areas suggests. And yet, it is also clear that the PFC is critical for supporting more abstract reasoning and planning abilities, including the ability to ignore distraction and other influences in the pursuit of a given goal. We will try to unravel the mystery of this seemingly contradictory coexistence of abilities in the PFC in this chapter.
Evidence for the importance of the PFC in higher-level cognitive control comes from the environmental dependency syndrome associated with damage to PFC. In one classic example, a patient with PFC damage visited a researcher's home and, upon seeing the bed, proceeded to get undressed (including removal of his toupee!), got into bed, and prepared to sleep. The environmental cues overwhelmed any prior context about what one should do in the home of someone you don't know very well. In other words, without the PFC, behavior is much more reflexive and unthinking, driven by the affordances of the immediate sensory environment, instead of by some more abstract and considered plan or goals. You don't need actual PFC damage to experience this syndrome -- certainly you have experienced yourself absent-mindedly doing something cued by the immediate sensory environment that you hadn't otherwise planned to do (e.g., brushing your teeth a second time before going to bed because you happened to see the toothbrush). We all experience lapses in attention -- the classic stereotype of an absent-minded professor is not explained by lack of PFC in professors, but rather that the PFC is apparently working on something else and thus leaves the rest of the brain to fend for itself in an environmentally-dependent manner.
Another great source of insight into the cognitive contributions of the PFC is available to each of us every night, in the form of our dreams. It turns out that the PFC is one of the brain areas most inactivated during dreaming phases of sleep. As a result, our dreams often lack continuity, and seem to jump from one disconnected scene to another, with only the most tangential thread connecting them. For example, one moment you might be reliving a tense social situation from high school, and the next you're trying to find out when the airplane is supposed to leave, with a feeling of general dread that you're hopelessly late for it.
So what makes the PFC uniquely capable of serving as the brain's executive? Part of the answer is its connectivity, as alluded to above -- it sits on top of the overall information processing hierarchy of the brain, and thus receives highly-processed "status reports" about everything important going on in your brain. In this sense it is similar to the hippocampus as we saw in the Memory Chapter, and indeed these areas appear to work together. However, the PFC is also especially well placed to exert control over our actions -- the PFC is just in front of the frontal motor areas (see the Motor Chapter), and has extensive connectivity to drive overt (and covert) motor behavior. Furthermore, the medial and ventral areas of PFC are directly interconnected with affective processing areas in subcortical regions such as the amygdala, thus enabling it to be driven by, and reciprocally, to amplify or override, motivational and affective signals.
In addition to being in the right place, the PFC also has some special biological properties that enable it to hold onto information in the face of distraction, e.g., from incoming sensory signals. Thus, with an intact PFC, you can resist the idea of laying down in someone else's bed, and remain focused on the purpose of your visit. We refer to this ability as robust active maintenance because it depends on the ability to keep a population of neurons actively firing over the duration needed to maintain a goal or other relevant pieces of information. This ability is also referred to as working memory, but this latter term has been used in many different ways in the literature, so we are careful to define it as synonymous with robust active maintenance of information in the PFC, in this context. We will see later how active maintenance works together with a gating system that allows us to hold in mind more than one item at a time, to selectively update and manipulate some information while continuing to maintain others, in a way that makes the integrated system support more sophisticated forms of working memory.
Recordings of neurons in the PFC of monkeys in the 1970's showed that they exhibit this robust active firing over delays (aka delay period activity). One of the most widely-used tasks is the oculomotor delayed response task, where a stimulus is flashed in a particular location of a video display, but the monkey is trained to maintain its eyes focused on a central fixation cross until that cross goes off, at which point it must then move its eyes to the previously flashed location in order to receive a juice reward. Neurons in the frontal eye fields (an area of PFC) show robust delay-period firing that is tuned to the location of the stimulus, and this activity terminates just after the monkey correctly moves its eyes after the delay. There are many other demonstrations of this robust active maintenance in the PFC of humans as well.
The computational models we explore in this chapter show how these two factors of connectivity and robust active maintenance can combine to support a wide range of executive function abilities that have been attributed to the PFC. The goal is to provide a unifying model of executive function, as compared to a laundry list of cognitive abilities that it is thought to support.
One of the most important executive function abilities is the ability to rapidly shift behavior or thought in a strategic manner (often referred to as cognitive flexibility). For example, when attempting to solve a puzzle or other challenging problem, you often need to try out many different ideas before discovering a good solution. Without the PFC, behavior is repetitive and stereotypical (banging your head against the wall again and again), lacking this hallmark flexibility. The ability to rapidly update what is being actively maintained in the PFC is what enables the PFC system to rapidly shift behavior or thought -- instead of requiring relatively slow synaptic weight modification to change how the system behaves, updating the pattern of active neural firing in PFC can change behavior immediately. In short, the PFC system contributes to behavioral adaptation by dynamically updating activation states, which then shape posterior cortical representations or motor actions via top-downbiasing of the associated patterns of activity. In contrast, behavioral adaption in the posterior cortex or basal ganglia relies much more on slowly adapting weight changes. Evidence for this difference comes from task switching paradigms, including the widely-studied Wisconsin card sorting task (WCST) in adults, and the dimensional change card sorting task (DCCS) in children.
The computational models in this chapter show how the basal ganglia (BG) and midbrain dopamine areas (specifically the ventral tegmental area, VTA) play a critical role in the rapid, strategic updating of PFC activity states. Specifically, we'll see that robust active maintenance requires an additional control signal to switch between maintaining existing information vs. updating to encode new information. The BG, likely in conjunction with dopaminergic signals from the VTA, play this role of dynamic gating of the maintenance of information in PFC. This dynamic gating function is identical to the role the BG plays in gating motor actions, as we saw in the Motor Chapter. Furthermore, the BG learning process is also identical to that in the Motor chapter based on reinforcement learning principles. Specifically, dopamine (from the SNc, which is next door to the VTA) shapes BG learning and thereby enables the gating mechanism to deal with the challenging problem of deciding what is important to maintain (and as such is task-relevant and therefore predictive of intrinsic reward), vs. what can be ignored (because it is not predictive of good task performance). These mechanisms embody the general notion that the PFC-BG cognitive system evolved by leveraging existing powerful mechanisms for gating motor behavior and learning. From this perspective, cognition cannot be divorced from motivation, as dopaminergic learning signals play a central and intimate role in the basic machinery of PFC/BG function. The analogous functions of BG and dopamine in cognitive and motor action selection and learning have been strongly supported by various data over the last 10 or 20 years, including evidence from monkey studies, and in humans, effects of disease impacting BG and/or dopamine, pharmacological manipulations, functional imaging, and genetics.