Cortical activations during paced finger-tapping applying visual and auditory pacing stimuli

Abstract

In order to study neural systems which are involved in motor timing we used whole-brain functional resonance imaging while subjects performed a paced finger-tapping task (PFT) with their right index finger. During one condition, subjects were imaged while tapping in synchrony with tones separated by a constant interval (auditory synchronisation, AS), followed by tapping without the pacing stimulus (auditory continuation, AC). In another condition, subjects were imaged while tapping in synchrony with a visual stimulus presented at the same frequency as the tones (visual synchronisation, VS) followed by a tapping sequence without visual pacing (visual continuation, VC). The following main results were obtained: (1) tapping in the context of visual pacing was generally more variable than tapping in the context of auditory stimuli; (2) during all conditions, a fronto-parietal network was active including the dorsal lateral premotor cortex (dPMC), M1, S1, inferior parietal lobule (LPi), supplementary motor cortex (SMA), the right cerebellar hemisphere, and the paravermial region; (3) stronger activation in the bilateral ventral premotor cortex (vPMC), the left LPi, the SMA, the right inferior cerebellum, and the left thalamus during both auditory conditions (AS and AC) compared to the visual conditions (VS and VC); (4) stronger activation in the right superior cerebellum, the vermis, and the right LPi during the visual conditions (VS and VC); (5) similar activations for the AS and AC conditions; but (6) marked differences between the VS and VC conditions especially in the dorsal premotor cortex (dPMC) and LPi areas; and (7) finally, there were no activations in the auditory and visual cortices when the pacing stimuli were absent. These findings were taken as evidence for a general difference between the motor control modes operative during the auditory and visual conditions. Paced finger tapping in the context of auditory pacing stimuli relies more on brain structures subserving internal motor control while paced finger-tapping in the context of visual pacing stimuli relies on brain structures relying on the subserving processing or imagination of visual pacing stimuli.

Introduction

It is generally accepted that motor control involves at least two discernible mechanisms, one of which is concerned with the control of movements in the spatial domain and the other with movement timing. In order to study movement timing, the paced finger-tapping (PFT) task is often used in which subjects produce a series of isochronous finger taps, first in synchrony with an external pacing stimulus (synchronisation, S) and then continuing on their own (continuation, C). Some of these studies seem to support the existence of an internal time-keeping system that is thought to be independent of external feedback mechanisms [48], [50]. Other studies support the contrasting notion that taps are synchronised with the external pacing stimuli at the central level by superimposing in time two sensory codes: a tactile/kinaesthetic code that represents the tap (the afferent movement code) and an auditory code that represents the click (the afferent code that results from the guiding signal). It is thus argued that external feedback may play a substantial role for the timing of isochronous taps [2]. Research in patients has linked control of motor timing to a number of motor structures, including the lateral cerebellum and its primary output nucleus, the dentate nucleus [18], [19], the basal ganglia [34], [39], [38], and the supplementary motor area (SMA) [15].

Two recent brain imaging studies employing the PFT paradigm provided results supporting the view that the lateral cerebellar cortex as well as the basal ganglia are involved in the production of timed motor responses. In the study of Rao et al. [40] subjects were imaged applying whole-head functional magnetic resonance imaging (fMRI) while tapping with their right index finger in synchrony with tones separated by two intervals. The results of their study suggest that the internal generation of precisely timed movements is dependent on three interrelated neural systems, one that is involved in explicit timing (putamen, ventrolateral thalamus, SMA), one that mediates auditory sensory memory (inferior frontal gyrus, IFG; superior temporal gyrus, STG), and another that is involved in sensorimotor processing (dorsal dentate nucleus, sensorimotor cortex). A most interesting result of their study is that the right auditory cortex together with the right inferior frontal gyrus is active during the continuation condition in which no explicit auditory pacing stimulus is present. Thus, these results support the notion that in a situation where external sensory input is lacking, a kind of internal generation of the auditory pacing stimuli might take place. A further main result of their study was that SMA as well as cerebellar activation was stronger for the continuation condition, although that was not explicitly tested. In a second brain imaging study (PET technique) related to that topic, Penhune et al. [36] applied auditory and visual pacing stimuli in the context of a PFT paradigm, without, however, using a continuation condition. Their results provide support for a supramodal contribution (independent of stimulus modality) of the lateral cerebellar cortex and cerebellar vermis to the production of a timed motor response. They also gave partial support to the involvement of the basal ganglia in motor timing. In addition, they demonstrated that sensory association areas and the ventromedial frontal cortex were involved in modality-specific encoding of the temporal pacing stimuli. Unfortunately, they did not use a continuation condition which would have allowed to confirm the findings of the Rao et al. study [40]. Furthermore, it would be interesting to know whether the visual cortex is active during a continuation condition, similar to the auditory continuation condition in the study of Rao et al.

Because there are partly conflicting results and some questions unanswered we designed the present study. The research questions are, in particular: (1) to delineate those brain structures which are involved in the control of the PFT task; (2) whether there are differences between auditory and visual pacing conditions in terms of activated brain areas; and (3) to test whether the visual continuation condition is indeed associated with increased activation in visual sensory areas. We thus designed an fMRI experiment in which subjects reproduced an isochronous tapping sequence paced by auditory and visual stimuli and were instructed to continue tapping when these stimuli were discontinued. Similar to the study of Penhune et al. [36] we predicted that if timing is a central process, the activation pattern should be closely similar for the two modalities. In line with the findings of Rao et al. [40], we further predicted that the auditory and visual cortex is active during the auditory and visual continuation conditions.