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. 2009 Aug 15;47(2):667-77.
doi: 10.1016/j.neuroimage.2009.04.065. Epub 2009 May 3.

Effects of timing and movement uncertainty implicate the temporo-parietal junction in the prediction of forthcoming motor actions

Oliver Jakobs  1 , Ling E Wang, Manuel Dafotakis, Christian Grefkes, Karl Zilles, Simon B Eickhoff
Affiliations

Effects of timing and movement uncertainty implicate the temporo-parietal junction in the prediction of forthcoming motor actions

Oliver Jakobs et al. Neuroimage. .

Abstract

The concept of predictive coding supposes the brain to build predictions of forthcoming events in order to decrease the computational load, thereby facilitating efficient reactions. In contrast, increasing uncertainty, i.e., lower predictability, should increase reaction time and neural activity due to reactive processing and believe updating. We used functional magnetic resonance imaging (fMRI) to scan subjects reacting to briefly presented arrows pointing to either side by pressing a button with the corresponding index finger. Predictability of these stimuli was manipulated along the independently varied factors "response type" (known hand or random, i.e., unknown order) and "timing" (fixed or variable intervals between stimuli). Behavioural data showed a significant reaction-time advantage when either factor was predictable, confirming the hypothesised reduction in computational load. On the neural level, only the right temporo-parietal junction showed enhanced activation upon both increased task and timing uncertainty. Moreover, activity in this region also positively correlated with reaction time. There was, however, a dissociation between both factors in the frontal lobe, as increased timing uncertainty recruited right BA 44, whereas increased response uncertainty activated the right ventral premotor cortex, the pre-SMA and the DLPFC. In line with the theoretical framework of predictive coding as a load-saving mechanism no brain region showed significantly increased activity in the lower uncertainty conditions or correlated negatively with reaction times. This study hence provided behavioural and neuroimaging evidence for predictive motor coding and points to a key role of the right temporo-parietal junction in its implementation.

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Figures

Fig. 1.
Fig. 1.
Left panel: Mean reaction times for the six experimental conditions. In the unilateral conditions, uncertainty in timing results in significant slower reaction times. Uncertainty of the response type also produced significant slower reaction times. Comparing fixed and jittered presentation of randomly pointing arrows, however, we observed no significant differences in reaction time. Right panel: Mean percentages of correct responses for the six experimental conditions. A significant main effect was only found for response type uncertainty.
Fig. 2.
Fig. 2.
(a) Pattern of activation for right-hand movements consisting of left primary motor and somatosensory cortex, thalamus and insula as well as bilateral secondary somatosensory cortex, basal ganglia, supplementary motor area, dorsal and ventral premotor cortices. Furthermore the right temporo-parietal junction and middle frontal gyrus were activated. For left hand movements we found a mainly mirror-reversed pattern of activity (b). Random hand movements (c) feature bilateral activation of the primary sensory-motor and cortex, putamen, pre-supplementary and supplementary motor area, ventral premotor cortex, cingulate motor cortex as well as the intraparietal sulcus and temporo-parietal junction. An additional bilateral cluster is localised on the superior frontal gyrus anterior to BA 6. Right-hemispheric activation was observed in pars opercularis of the right inferior frontal gyrus (BA 44). (d) Areas which have been constantly active throughout all condition and hence represent the “core motor areas”. Activity was found bilateral in the dorsal premotor cortex, the mesial aspect of the frontal lobe (SMA) and the putamen.
Fig. 3.
Fig. 3.
Uncertainty about the subsequent movement caused increased activity in bilateral pre-supplementary cortex, superior frontal gyrus anterior to BA6 (SFG) and the intraparietal sulcus. Right-hemispheric activation was observed in the temporo-parietal junction, the dorso-lateral prefrontal cortex and ventral premotor cortex. The reverse contrast (unilateral>random hands) did not yield any significant activations.
Fig. 4.
Fig. 4.
The right inferior frontal gyrus (BA 44) as well as the right temporo-parietal junction (Area PF) show increasing activity when contrasting unilateral conditions with fixed and respectively jittered timing. The activated temporo-parietal region (60/−38/15) overlaps with the region activated when contrasting conditions with respectively unilateral and random hand movements (Fig. 3). No region was associated with reduced timing uncertainty.
Fig. 5.
Fig. 5.
This picture illustrates the differential activation of frontal areas associated with the main effects of experimental factors (response type=red, timing uncertainty=green). Increasing uncertainty of movement direction activates the right ventral premotor cortex whereas increasing uncertainty of timing produces activation of a region into BA 44. These two activations are hence functionally and anatomically distinct from each other.
Fig. 6.
Fig. 6.
Testing for correlations between neuronal activity and reaction-time differences we observed activation in temporo-parietal Area PF (60/−38/15) overlapping with those found for increased uncertainty in movement direction and timing despite orthogonalising the covariate by condition. Increasing reaction times represent the behavioral indicator for processing speed and computational load. Considering the parietal activation pattern in the different contrasts and the behavioral data we propose that Area PF is mainly involved in updating movement plans in the predictive coding framework.
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