From preparation to online control: Reappraisal of neural circuitry mediating internally generated and externally guided actions

Abstract

Action plans internally generated (IG) from memory are thought to be regulated by the supplementary motor area (SMA), whereas plans externally guided (EG) online using sensory cues are believed to be controlled by the premotor cortex. This theory was investigated in an event-related fMRI study that separated the time course of activation before and during movement to distinguish advance planning from online control. In contrast to prevailing theory, the SMA was not more important for online control of IG actions. EG movement was distinguished from IG movement by greater activation in a more distributed right hemisphere parietal–frontal network than previously reported. Comparisons between premovement and movement periods showed that frontostriatal networks are central for preparing actions before movement onset. However, unlike cortical and cerebellar regions, the basal ganglia exhibited planning-related activity before, but not during, movement. These findings indicate that the basal ganglia mediate planning and online control processes in different ways and suggest a specific role for the striatum in internally planning sequences of actions before they are implemented.

Introduction

Humans are remarkably proficient at learning large repertoires of skills, nearly all aspects of which require sequencing actions. Central to controlling action sequences are planning operations, which encompass a broad range of cognitive processes that allow us to anticipate events, select movements, specify their ordering, and control actions online. Plans for some sequential behaviors, like performing the tango, are internally generated (IG) since dance steps are implemented by retrieving a memory representation of an action sequence that fits the music. Plans for other sequential behaviors, like stepping on the brakes and steering to avoid an oncoming car, are externally guided (EG) because the actions are strongly associated with visual or other sensory cues that dictate when and how to act. It remains a matter of considerable debate, however, as to whether IG and EG actions involve fundamentally different planning processes that are mediated by distinct brain systems. The prospect that IG and EG movements come under different neural control is suggested by the observation that people with Parkinson's disease have problems performing movements generated from memory but often overcome this difficulty when provided with an external sensory cue (Glickstein and Stein, 1991).

To explore this issue, previous studies have used “free-movement”, “free-selection”, or “spontaneous willed-action” tasks wherein different movements or sequences of movements are self-generated on each trial (Hunter et al., 2003). Functional activity during these tasks is contrasted with tasks in which the same movements are guided by auditory or visual cues. An assumption is that plans for IG actions are intention-based because they are driven by an internal “urge” or desire whereas plans for EG actions are stimulus-based because they are guided online by external cues. The common finding is that supplementary motor area (SMA) activation is greater during IG movement and lateral premotor activation is greater during EG movement (Jenkins et al., 2000, Tanji, 1996). This suggests that the SMA is crucial for planning and executing actions generated from memory whereas the lateral premotor cortex mediates planning movements that are guided by visual or other sensory cues (Goldberg, 1985).

Still, evidence supporting neuroanatomically distinct mechanisms for these two routes to action is limited in part because the tasks used to study IG behaviors place greater demands on processes that are only peripherally related to planning movements from memory. This is because in IG tasks the subject selects an action from a repertoire of behaviors, with the constraint that the same action cannot be repeated on successive trials. For this reason, differences in activation patterns between IG and EG actions may be more related to the greater demands of IG actions on maintaining and updating working memory, attending to multiple actions, and/or response conflict monitoring (Lau et al., 2004). It has also been difficult to elucidate distinct neural mechanisms for intention- and stimulus-based planning because in the laboratory IG and EG actions are highly predictable since the repertoire of potential movements is typically quite small (e.g., one or two movements) to ensure that both types of actions are equivalent. As a consequence, IG actions are partly stimulus-guided in that they are well specified by external task instructions rather than “spontaneously” generated as sometimes implied. In fact, the distinction between these two routes of action may be overdrawn in the laboratory and real world (Waszak et al., 2005) since IG behaviors require some level of stimulus guidance from the environment to specify actions for a behavioral context. Similarly, though EG actions are guided online by stimulus information, they require some internal planning. Thus, a more pivotal distinction may be that IG-generated behaviors are planned and implemented from memory whereas EG behaviors are planned online with the aid of sensory information.

In the present study, subjects underwent event-related fMRI while performing IG and EG motor sequences. We asked whether IG and EG actions are modulated by neuroanatomically distinct mechanisms when executive processing demands of IG movements are minimized. To investigate this question, we focused on a central difference between the two routes to action, namely that IG action plans are prepared, retrieved, and implemented from memory whereas EG action plans are formulated online using sensory cues to guide performance. To increase planning and online control demands, a large repertoire of actions (i.e., 9 different sequences) was used so that movements were not highly predictable from trial to trial. We also separated the time course of activation associated with planning and executing movements, which enabled us to (1) identify the neural systems that were associated with planning IG movements and holding them in memory (IG premovement) from those involved in motor readiness/anticipation (EG premovement) and (2) determine whether the neural control of IG and EG actions differed during movement (IG versus EG movement). This design also allowed us to distinguish neural systems principally associated with generating action plans (IG premovement) from those involved in retrieving and implementing plans from memory (IG movement). Despite its theoretical importance, this issue has received little consideration in neuroimaging studies of motor control. Unlike previous studies, two levels of sequence complexity were also used to identify differences in neural activation patterns associated with increased difficulty in advanced planning and online control (Harrington et al., 2000). We reasoned that sequence complexity should exert a differential effect on brain activation for IG and EG sequences during movement if they differ in the difficulty of online control processes. Similarly, regions principally associated with formulating plans in memory should show a greater effect of sequence complexity before movement (IG premovement), whereas those more involved in retrieving and implementing plans from memory should show a greater effect of sequence complexity during movement (IG movement).