The neural correlates of speech motor sequence learning

Abstract

Speech is perhaps the most sophisticated example of a species-wide movement capability in the animal kingdom, requiring split-second sequencing of approximately 100 muscles in the respiratory, laryngeal, and oral movement systems. Despite the unique role speech plays in human interaction and the debilitating impact of its disruption, little is known about the neural mechanisms underlying speech motor learning. Here, we studied the behavioral and neural correlates of learning new speech motor sequences. Participants repeatedly produced novel, meaningless syllables comprising illegal consonant clusters (e.g., GVAZF) over 2 days of practice. Following practice, participants produced the sequences with fewer errors and shorter durations, indicative of motor learning. Using fMRI, we compared brain activity during production of the learned illegal sequences and novel illegal sequences. Greater activity was noted during production of novel sequences in brain regions linked to non-speech motor sequence learning, including the BG and pre-SMA. Activity during novel sequence production was also greater in brain regions associated with learning and maintaining speech motor programs, including lateral premotor cortex, frontal operculum, and posterior superior temporal cortex. Measures of learning success correlated positively with activity in left frontal operculum and white matter integrity under left posterior superior temporal sulcus. These findings indicate speech motor sequence learning relies not only on brain areas involved generally in motor sequencing learning but also those associated with feedback-based speech motor learning. Furthermore, learning success is modulated by the integrity of structural connectivity between these motor and sensory brain regions.

Figure 1

Behavioral results from syllable productions. The * symbol indicates significance of p_FWE < 0.05. A. Practice session results comparing behavior on day 1 and day 2 of practice. Mean error rate (top left) and utterance duration (bottom left) decreased significantly from day 1 to day 2 of practice for learned illegal (white) but not learned legal syllables (gray). The reduction in mean error rate (top right) and utterance duration (bottom right) was significantly greater for learned illegal syllables (gray) than learned legal syllables (white). B. Imaging session results. Left: Subjects produced learned legal (white) and learned illegal (light gray) syllables significantly more accurately than novel illegal syllables (dark gray). Right: Subjects produced learned illegal syllables significantly faster than novel illegal sequences, but slower than learned legal syllables. Bars indicate standard error.

Figure 2

FMRI main effects of speech motor sequence learning (novel illegal - learned illegal). Significant cortical clusters are shown on the left lateral (upper left), right lateral (upper right), and right medial (lower right) inflated cortical surface. The significant subcortical cluster is shown on the MNI305 template (bottom left), with the y coordinate of individual slices indicated; left and right hemispheres are indicated by L and R, respectively. Colors within the active clusters indicate the relative significance level of the effect at the underlying voxel/vertex (expressed as –log(p)). Abbreviations: FO = frontal operculum-anterior insula, GP = globus pallidus, ITO = inferior temporal-occipital cortex, PMC = premotor cortex, preSMA = pre-supplementary motor area, pSTg = posterior superior temporal gyrus, pSTs = posterior superior temporal sulcus, SPL = superior parietal lobule.

Figure 3

FMRI main effects of consonant cluster phonotactic legality in practiced syllables (learned illegal - learned legal). Significant cortical clusters are shown on the left lateral (upper left), right lateral (upper right), and left medial (lower left) inflated cortical surface. The significant subcortical cluster is shown on a slice through the cerebellum at y=-60 in the MNI305 template (bottom right); left and right hemispheres are indicated by L and R, respectively. Colors within the active clusters indicate the significance level of the effect at the underlying voxel/vertex (expressed as –log(p)). Abbreviations: ITO = inferior temporal-occipital cortex, OC = occipital cortex, PMC = premotor cortex, pSTg = posterior superior temporal gyrus, SMA = supplementary motor area, SMg = supramarginal gyrus, SPL = superior parietal lobule.

Figure 4

Neural markers of learning success. Left. Significant correlation between individual learning success and the novel illegal - learned illegal syllable BOLD activity within the left frontal operculum-anterior insula cluster (FO; r = 0.709, p_FWE = 0.029). Middle. Significant correlation between learning success and the mean fractional anisotropy underlying the left posterior superior temporal sulcus cluster (pSTs; r = 0.670, p_FWE = 0.040). Right. Locations for FO and pSTs used in the correlation analyses.

Figure 5

Schematic of the learning of a speech motor program for the consonant cluster /zv/. The left half of the figure represents the situation prior to practicing the new cluster. In this case, two separate motor programs (indicated by dashed lines), one for each consonant in the cluster, must be activated sequentially to produce the cluster. The right half of the figure represents the situation after repeated production of the consonant cluster. At this stage, a single motor program can be used to produce the cluster. See text for further details. Abbreviations: G = gesture, MC = motor cortex, MP = motor program, PMC = premotor cortex.