A network model of observation and imitation of speech

Abstract

Much evidence has now accumulated demonstrating and quantifying the extent of shared regional brain activation for observation and execution of speech. However, the nature of the actual networks that implement these functions, i.e., both the brain regions and the connections among them, and the similarities and differences across these networks has not been elucidated. The current study aims to characterize formally a network for observation and imitation of syllables in the healthy adult brain and to compare their structure and effective connectivity. Eleven healthy participants observed or imitated audiovisual syllables spoken by a human actor. We constructed four structural equation models to characterize the networks for observation and imitation in each of the two hemispheres. Our results show that the network models for observation and imitation comprise the same essential structure but differ in important ways from each other (in both hemispheres) based on connectivity. In particular, our results show that the connections from posterior superior temporal gyrus and sulcus to ventral premotor, ventral premotor to dorsal premotor, and dorsal premotor to primary motor cortex in the left hemisphere are stronger during imitation than during observation. The first two connections are implicated in a putative dorsal stream of speech perception, thought to involve translating auditory speech signals into motor representations. Thus, the current results suggest that flow of information during imitation, starting at the posterior superior temporal cortex and ending in the motor cortex, enhances input to the motor cortex in the service of speech execution.

Keywords: action observation; brain imaging; effective connectivity; language; mirror neuron; speech; structural equation modeling; ventral premotor cortex.

Figure 1

Activation during observation and imitation. Voxels were selected using general linear model after adjusting for false positives using false discovery rate (p < 0.05). The figure shows the data obtained from a representative single subject.

Figure 2

Observation and Imitation models in both the LH and RH with connections between pST, aST, IP, vPM, dPM, and M1S1. IP, inferior parietal lobule. M1S1, primary motor/somatosensory cortex; pST, posterior superior temporal gyrus and sulcus; aST, anterior superior temporal gyrus and sulcus; vPM, ventral premotor cortex; dPM, dorsal premotor cortex; M1/S1, primary motor/somatosensory cortex. Anatomical definitions of the regions are provided in Table 1.

Figure 3

Comparison between the models of observation and imitation in LH and in the RH. The connections between pST, aST, IP, vPM, dPM, and M1S1 showing stronger connection weights for Imitation vs Observation, and stronger connection weights for Observation vs Imitation. The flow of information in the LH might suggest a pathway to execute speech during Imitation. For a key to abbreviations, please see the legend to Figure 2 and Table 1.

Figure 4

Common pathways for observation and imitation in the LH. Observation and Imitation models in the LH with connections between pST, aST, IP, vPM, dPM, and M1S1. Black arrows show the connections that did not differ statistically across the Observation and Imitation models. For a key to abbreviations, please see the legend to Figure 2 and Table 1.