What and when: parallel and convergent processing in motor control

Abstract

Successful motor behavior requires making appropriate response (response selection) at the right time (timing adjustment). Earlier psychological studies have suggested that the response selection and timing adjustment processes are performed serially in separate stages. We tested this hypothesis using functional magnetic resonance imaging. The subjects performed a choice reaction time task in four conditions: two (on-line response selection required or not) by two (on-line timing adjustment required or not). We found that the neural correlates for the two processes were indeed separate: the anterior medial premotor cortex (presupplementary motor area) was selectively active in response selection, whereas the cerebellar posterior lobe was selectively active in timing adjustment. However, the functional separation was only partial in that the lateral premotor cortex and the intraparietal sulcus were active equally for response selection and timing adjustment. The lateral premotor cortex was most active when both processes were required, suggesting that it integrates the information on response selection and the information on timing adjustment; alternatively, it might contribute to the allocation of attentional resources during dual information processing. The intraparietal sulcus was equally active when either response selection or timing adjustment was required, suggesting that it modifies, rather than integrates, these processes. Furthermore, our results suggest that these activations related to response selection and timing adjustment were distinct from sensory or motor processes.

Fig. 1.

a, Scheme for reaction processes proposed in the earlier psychological studies (Frowein et al., 1981). The overall processes were thought to take several discrete stages arranged in a serial manner, where response uncertainty and time uncertainty independently affect the response selection and timing adjustment stages, respectively. In the original scheme, the timing adjustment was termed as motor adjustment. We used the present term to stress on the timing aspect. b, Task procedures. Subjects were asked to press buttons in response to the two types of stimuli using the index and middle finger of the right hand. The order of the presentation of the two types of stimuli and ISI were set either regular or random, creating four conditions named control, response uncertainty, time uncertainty, and dual uncertainty. c,Procedures for fMRI experiments. Six runs of experiments were conducted, three using the auditory paradigm, and the other three using the visual paradigm. For each run, one of the uncertainty, control, and rest conditions were repeated for six times in a counterbalanced order.

Fig. 2.

Reaction times (a) and variance of reaction times (b) for the four conditions: control (cont), response uncertainty (resp), time uncertainty (time), and dual uncertainty (dual). Means and the SEs for the six subjects were separately shown for the auditory (left) and visual (right) paradigms.

Fig. 3.

Statistical parametric analysis: sensory-modality-independent areas. Areas related to response selection and/or timing adjustment processes (a) and areas related to motor execution process (b) are shown in yellow on the surface of the standard brain (left three figures) and on the three axial slices of a single subject fitted into the Talairach space (Talairach and Tournoux, 1988) (right three figures). Theleft side of the figure indicates the left hemisphere.a, (response uncertainty–control) ∪ (time uncertainty–control) ∪ (dual uncertainty–control);b, (control–rest) ∩ (response uncertainty–rest) ∩ (time uncertainty–rest) ∩ (dual uncertainty–rest).

Fig. 4.

Region-based analysis. a, Seven volumes of interest placed on both hemispheres are shown on four slice images of one subject, which were determined based on the anatomical landmarks. Light pink, PreSMA/rCMA; dark pink, SMA-proper; light blue, PM; dark blue, M1; light green, Cbll-ant; dark green, Cbll-post; yellow, IPS. b,The active volume sizes under the four conditions, control (cont), response uncertainty (resp), time uncertainty (time), and dual uncertainty (dual), relative to rest are shown in cubic millimeters for the seven volumes of interest. The values were combined for both hemispheres and the means and SEs for the six subjects are indicated.

Fig. 5.

Statistical parametric analysis: sensory–modality-dependent areas. Areas of significant activation for the group of six subjects are indicated on the surface of the standard brain. a,Top row, (response uncertainty–control); second row, (time uncertainty–control); third row, (dual uncertainty–control); b, (control–rest) ∩ (response uncertainty–rest) ∩ (time uncertainty–rest) ∩ (dual uncertainty–rest).

Fig. 6.

Hypothetical neural mechanisms for the processing of response selection and timing adjustment; the processing (top) and the neural correlates (bottom). The scheme depicts the parallel processing of response selection and timing adjustment, which are subserved by PreSMA/rCMA and Cbll-post. PM may either integrate these kinds of information or allocate attentional resources during dual information processing.