Working Memory: The Foundation of Adaptive Behavior
Behavioral choices are continuously made by all vertebrate animals on a moment-by-moment basis (Cisek & Kalaska, 2010). Working memory (WM) plays an important and remarkable role in the selection of behavior, holding and processing potential perception-action linkages, with choices occurring in an ongoing manner. When an organism can identify behavior with the greatest chance of success and act within the environment to access that behavior, the result is optimal adaptation. This process occurs early in development, allowing for the gradual build-up of an extensive “knowledge base” of successful perception-action linkages, which are stored within a distributed brain network for future access when needed (Amso & Davidow, 2012; Davidson, Amso, Anderson, & Diamond, 2006). The basal ganglia and cerebellum are active from early infancy. An fMRI analysis of healthy infants during natural sleep identified a resting state network that encompassed the bilateral basal ganglia (Fransson et al., 2009). Similarly, a recent study revealed a dramatic myelination growth of the pons (the primary structure through which cortical projections enter the cerebellum) during early infancy (Tate et al., 2015).
Development progresses from reflexive behavior to perception-action linkages, and is based on interaction with the environment (Johnson, Ok, & Luo, 2007; Konicarova & Bob, 2013a, 2013b; Leisman, Braun-Benjamin, & Melillo, 2014; Tau & Peterson, 2010). Early experiences of “behavioral success” expand and build throughout infancy, childhood, adolescence and into adulthood. Infants are born with reflexes that help them to survive. Initially, a reflex is an adaptive response to a stimulus with no WM to guide it. The reflex is quickly reinforced, meaning the cortical-basal ganglia system identifies something that “works”. For example, consider how the sucking reflex becomes linked with food reward through a basic pattern that repeats and builds upon itself. And what is the pattern?
The action (e.g. sucking), becomes associated with a high probability of obtaining food, through the dopaminergic cortical-basal ganglia system.
At the same time, the cortical-cerebellar system makes a copy of the contents of cortical WM associated with the suck reflex as experienced within the environment. This results in the formation of anticipatory sensory and motor cues (e.g. sight and feel of the nipple; formation of the mouth movement for sucking).
Implicit WM processes combine with cortical-subcortical systems to form a perception-action linkage, resulting in a strong and lasting association between the sensory-motor behavior of sucking and the high probability of obtaining food.
The perception-action linkage is applied when new situations are encountered, leading to the formation of new perception-action linkages, such as using the mouth to suck from a straw or to chew.
There are many real-life illustrations of how WM is involved in the formation of perception-action linkages. The formation of mouth movements to smile or the vocal intonations to coo lead to warmth (e.g. body contact) and pleasurable social interactions (e.g. being picked up, played with, attended to). These likely lead to basal ganglia recognition of anticipatory reward combined with cerebellar automation of sensory-motor aspects of these behaviors, resulting in the storage of perception-action linkages within cortical structures.
Consider the role of implicit WM in applying previously learned perception-action linkages to a new skill. When a toddler learns to tie her shoes, implicit WM is required to hold a set of previously learned, fully automated skills to solve the new problem. For example, the pincer grasp is required to tie shoes. However, the pincer grasp was previously a completely novel task that required repeated practice to master. This practice involved a series of grasping movements and progressive approximations in preparation for mastery of the pincer grasp (Wallace & Whishaw, 2003). With practice and effort, the pincer grip becomes automated and effortless, a perception-action linkage called upon when faced with a new and unfamiliar task, like shoe tying. Certain cognitive concepts must also be automated prior to learning shoe tying, such as the spatial concepts of front and back. The child no longer has to “think” about these motor (pincer grasp) and spatial (front, back) skills, allowing her to focus effortful processing on learning the shoe tying skill. WM “holds” the previously learned perception-action linkages that are needed for mastery of the current novel task.
Explicit WM is also called upon as the child applies a “shoe tying rule” learned from her mother: “Cross the laces, one over the other.” This rule must be held in mind while attempting the task. WM is also involved in mastering a sequence of complex steps that must be held in during each attempt to practice the task. Sequencing involves the cortical-basal ganglia system (Hazy, Frank, & O'Reilly, 2006; Koziol & Budding, 2009; McNab & Klingberg, 2008). The ultimate goal is to fully automate the shoe tying skill. This occurs through practice and repetition, resulting in slow and gradual improvements in performance, a process that directly involves the cortical-cerebellar system. The cerebellum copies the contents of cortical WM, resulting in an internal model of shoe tying, then gradually corrects errors, sending correction signals to the cortex, where the improvements are stored. As error correction results in continued improvements in performance, cerebellar activation decreases (Flament, Ellermann, Kim, Ugurbil, & Ebner, 1996). The learning process may involve mastery of multiple smaller steps in a hierarchical fashion, such as learning to cross the laces, learning to make the loop for tying, etc.
At each step, both explicit and implicit WM is involved. The explicit WM involvement may include a verbal rule held in mind, or a mental image of the modeled ability. The implicit WM involvement includes the application of previously learned perception-action linkages that are held in mind while working towards mastery of the entire task. At each step in the learning process, the basal ganglia releases the necessary information into WM and inhibits unnecessary information. Anticipatory reward is also involved; the child previously earned praise from her mother when she successfully learned other skills, enabling the basal ganglia to predict future reward once the current shoe tying skill is mastered. Anticipatory reward may serve as a motivating factor as the child struggles with such a difficult and challenging task.
All behaviors involve chains of perception-action linkages. The “links in the chain” must be held in mind as new perception-action linkages are formed. This is a potentially useful idea that can be applied in a variety of clinical and research settings to better understand and treat problems associated with WM. The chains of perception-action linkages involve holding previously learned associations (e.g. various combinations of perceptions, ideas, and actions) in mind as newly learned associations are formed, resulting in the gradual increase of behavioral repertoire. These perception-action linkages develop through repetition. New behavior must be attempted many times before the behavior becomes routine.
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