Relative Contributions of the Dorsal vs. Ventral Speech Streams to Speech Perception are Context Dependent: a lesion study

• ¹ Arizona State University, United States
• ² University of Iowa, United States
• ³ University of California, Irvine, United States
• ⁴ University of Southern California, United States
• ⁵ Medical College of Wisconsin, United States
• ⁶ San Diego State University, United States

The neural basis of speech perception has been debated for over a century. While it is generally agreed that the superior temporal lobes are critical for the perceptual analysis of speech, a major current topic is whether the motor system contributes to speech perception, with several conflicting findings attested. In a dorsal-ventral speech stream framework (Hickok & Poeppel 2007), this debate is essentially about the roles of the dorsal versus ventral speech processing streams. A major roadblock in characterizing the neuroanatomy of speech perception is task-specific effects. For example, much of the evidence for dorsal stream involvement comes from syllable discrimination type tasks, which have been found to behaviorally doubly dissociate from auditory comprehension tasks (Baker et al. 1981). Discrimination task deficits could be a result of difficulty perceiving the sounds themselves, which is the typical assumption, or it could be a result of failures in temporary maintenance of the sensory traces, or the comparison and/or the decision process. Similar complications arise in perceiving sentences: the extent of inferior frontal (i.e. dorsal stream) activation during listening to sentences increases as a function of increased task demands (Love et al. 2006). Another complication is the stimulus: much evidence for dorsal stream involvement uses speech samples lacking semantic context (CVs, non-words). The present study addresses these issues in a large-scale lesion-symptom mapping study. 158 patients with focal cerebral lesions from the Mutli-site Aphasia Research Consortium underwent a structural MRI or CT scan, as well as an extensive psycholinguistic battery. Voxel-based lesion symptom mapping was used to compare the neuroanatomy involved in the following speech perception tasks with varying phonological, semantic, and task loads: (i) two discrimination tasks of syllables (non-words and words, respectively), (ii) two auditory comprehension tasks, (iii) two sentence comprehension tasks (sentence-picture matching, plausibility judgments), and (iv) two sensory-motor tasks (a non-word repetition task and BDAE repetition subtest). Our results indicate that the neural bases of speech perception are task-dependent. The syllable discrimination and sensory-motor tasks all identified a dorsal temporal-parietal voxel cluster, including area Spt, primary auditory and somatosensory cortex. Conversely, the auditory comprehension task identified left mid-temporal regions. This suggest that syllable discrimination deficits do not stem from impairments in the perceptual analysis of speech sounds but rather involve temporary maintenance of the stimulus trace and/or the similarity comparison process. The ventral stream (anterior and posterior clusters in the superior and middle temporal gyri), were associated with both sentence tasks. However, the dorsal stream’s involvement was more selective: inferior frontal regions were identified in the sentence–to-picture matching task, not the semantic plausibility task. Within the sentence-to-picture matching task, these inferior frontal regions were only identified by the trials with the most difficult sentences. This suggests that the dorsal stream’s contribution to sentence comprehension is not driven by perception per se. These initial findings highlight the task-dependent nature of speech processing, challenge claims regarding any specific motor region being critical for speech perception, and refute the notion that speech perception relies on dorsal stream auditory-motor systems.