Neural correlates of visuomotor adjustments during scaling of human finger movements

Abstract

Visually guided finger movements include online feedback of current effector position to guide target approach. This visual feedback may be scaled or otherwise distorted by unpredictable perturbations. Although adjustments to visual feedback scaling have been studied before, the underlying brain activation differences between upscaling (visual feedback larger than real movement) and downscaling (feedback smaller than real movement) are currently unknown. Brain activation differences between upscaling and downscaling might be expected because within-trial adjustments during upscaling require corrective backwards accelerations, whereas correcting for downscaling requires forward accelerations. In this behavioural and fMRI study we investigated adjustments during up- and downscaling in a target-directed finger flexion-extension task with real-time visual feedback. We found that subjects made longer and more complete within-trial corrections for downscaling perturbations than for upscaling perturbations. The finger task activated primary motor (M1) and somatosensory (S1) areas, premotor and parietal regions, basal ganglia, and cerebellum. General scaling effects were seen in the right pre-supplementary motor area, dorsal anterior cingulate cortex, inferior parietal lobule, and dorsolateral prefrontal cortex. Stronger activations for down- than for upscaling were observed in M1, supplementary motor area (SMA), S1 and anterior cingulate cortex. We argue that these activation differences may reflect differing online correction for upscaling vs. downscaling during finger flexion-extension.

The role of the cerebellum in adaptation: ALE meta‐analyses on sensory feedback error

“…Among studies that implemented a continuous shift of feedback, six activations were in lobule VI (Brand et al, 2017;Diedrichsen et al, 2005;Grafton et al, 2008;Graydon et al, 2005;Inoue et al, 2000;Zheng et al, 2013), three in lobule VIII (Anguera et al, 2010;Krakauer et al, 2004;Tourville et al, 2008), with two foci just anterior to Lobule VI in the IV/V region (Anguera et al, 2010;Seidler et al, 2006), and two in Crus I/II (Krakauer et al, 2004). The same regions were reported for studies of mismatched feedback, with three foci incorporated in Lobule VI (Pfordresher et al, 2014;Tunik et al, 2013;Yomogida et al, 2010), two in Crus II (Pfordresher et al, 2014;Schnell et al, 2007), and one in Lobule VIII (Pfordresher et al, 2014).…”

“…The anterior map is centered on lobule VI, while the posterior is centered on lobule VIII. The majority of cerebellar activations in studies included in our analyses were reported in lobules VI (Brand et al, ; Diedrichsen et al, ; Grafton et al, ; Graydon et al, ; Inoue et al, ; Pfordresher et al, ; Tunik et al, ; Yomogida et al, ; Zheng et al, ), and VIII (Anguera et al, ; Krakauer et al, ; Pfordresher et al, ; Tourville et al, ). This demonstrates that where cerebellar activations were observed they were not distributed randomly, making these findings unlikely to be false positives.…”

“…For example, shifted and feedback mismatch studies were twice as likely to elicit cerebellar activity than not (12/18 and 4/6), while temporal manipulations only elicited cerebellar activity in a quarter of the respective experiments (2/8). Among studies that implemented a continuous shift of feedback, six activations were in lobule VI (Brand et al, ; Diedrichsen et al, ; Grafton et al, ; Graydon et al, ; Inoue et al, ; Zheng et al, ), three in lobule VIII (Anguera et al, ; Krakauer et al, ; Tourville et al, ), with two foci just anterior to Lobule VI in the IV/V region (Anguera et al, ; Seidler et al, ), and two in Crus I/II (Krakauer et al, ). The same regions were reported for studies of mismatched feedback, with three foci incorporated in Lobule VI (Pfordresher et al, ; Tunik et al, ; Yomogida et al, ), two in Crus II (Pfordresher et al, ; Schnell et al, ), and one in Lobule VIII (Pfordresher et al, ).…”

“…This type of motor learning therefor must not be seen as planning new coordinated motor plans, and instead viewed specifically as reoptimization that seeks to minimize future costs to the motor system by forming more accurate predictions of existing motor plans (Izawa, Rane, Donchin, & Shadmehr, 2008). Across the studies in our analyses, cerebellar foci were most common in studies driving adaptation in response to physical perturbation of the mouth (Golfinopoulos et al, 2011) and arm (Diedrichsen et al, 2005), learning new associations between the spatial consequences of movement when visual feedback is shifted (Anguera et al, 2010;Brand et al, 2017;Diedrichsen et al, 2005;Grafton et al, 2008;Graydon et al, 2005;Inoue et al, 2000;Krakauer et al, 2004;Seidler et al, 2006;Zheng et al, 2013), and when vocal pitch was shifted during continuous speech (Tourville et al, 2008;Zheng et al, 2013). All of these manipulations evoke the fine-tuning of accurately predicting movement outcomes in response to changes in the environment (Ishikawa et al, 2016).…”

A comprehensive study on the cognitive mechanisms and neural substrates of hallucination proneness

“…The anterior map is centred on lobule VI, while the posterior is centred on lobule VIII. The majority of cerebellar activations in studies included in our analyses were reported in lobules VI (Brand et al, 2017;Diedrichsen et al, 2005;Grafton et al, 2008;Graydon et al, 2005;Inoue et al, 2000;Pfordresher et al, 2014;Tunik et al, 2013;Yomogida et al, 2010;Zheng et al, 2013), and VIII (Anguera et al, 2010;Krakauer et al, 2004;Pfordresher et al, 2014;Tourville et al, 2008). This demonstrates that where cerebellar activations were observed they were not distributed randomly, making these findings unlikely to be false positives.…”