Rationale:
Recent investigations into the organization of the human auditory system have identified cortical areas that are specialized for processing a variety of different categories of sound, including speech, language, and music. Furthermore, research in nonhuman primates has yielded insights into the anatomical connections that define auditory cortex, and the pathways along which information is thought to propagate. However, there is a lack of functional evidence for these anatomical pathways in humans due to the difficulty in recording neural activity from wide cortical areas with high spatial and temporal resolution. Such recordings are currently only possible in patients undergoing temporary placement of electrocorticographic grids (ECoG), typically to develop a neurosurgical plan to treat intractable epilepsy. Our current research seeks to evaluate human ECoG responses to auditory speech stimuli to validate the caudal to rostral activity progression expected from nonhuman primate studies and to provide clinicians with functional maps of this progression.
Method:
We recruited 13 human subjects with intractable epilepsy who underwent surgical implantation of subdural ECoG electrodes over their temporal lobe (1-2.3 mm exposed diameter, 3-10 mm pitch). Subjects were presented with a random sequence of lyrical music, native speech, and foreign speech stimuli, which were 2 seconds in duration with a variable 1.4-1.8 second silent inter-stimulus period. In our analysis, we identified those cortical areas that responded to the auditory stimuli by measuring the stimulus-induced increase in spectral power within the high gamma (70-170 Hz) frequency band. Next, we determined the onset of population-level cortical activity in single trials for the activity exhibited by these electrodes (see Figure 1). We used the median onset latency at each location to develop a linear model that describes the relationship between the location of the electrode along the axis of the superior temporal gyrus (STG) and the onset latency of that location.
Results:
As expected, our results localize auditory responses primarily to the STG. We found the earliest onset of cortical activity around 170 ms after stimulus onset. Most importantly, our results show a clear temporal progression from caudal to rostral parts of the STG for speech stimuli. This progression was most prominent for native speech (0.54) followed by foreign speech (0.52) and lyrical music (0.47, r-squared values).
Conclusion:
Our study provides evidence that ECoG recordings can highlight a detailed temporal progression of information within the human auditory system and documents a caudal to rostral information flow in speech processing. Further studies can expand this analysis to higher-level processing of language content within speech stimuli, and translate this temporal information into a useful tool for mapping of speech and language function in patients undergoing resective brain surgery.
Funding:
:This work was supported by the NIH/NIBIB (P41-EB018783, R01-EB026439), the NIH/NINDS (U01-NS108916 and U24-NS109103), the NIH/NIMH (P50-MH109429), the NIH/NICHD (DP1-HD091947) and Fondazione Neurone. We thank all the patients who participated in the study.
FIGURES
Figure 1