Functional significance of the electrocorticographic auditory responses in the premotor cortex

Abstract

Other than well-known motor activities in the precentral gyrus, functional magnetic resonance imaging (fMRI) studies have found that the ventral part of the precentral gyrus is activated in response to linguistic auditory stimuli. It has been proposed that the premotor cortex in the precentral gyrus is responsible for the comprehension of speech, but the precise function of this area is still debated because patients with frontal lesions that include the precentral gyrus do not exhibit disturbances in speech comprehension. We report on a patient who underwent resection of the tumor in the precentral gyrus with electrocorticographic recordings while she performed the verb generation task during awake brain craniotomy. Consistent with previous fMRI studies, high-gamma band auditory activity was observed in the precentral gyrus. Due to the location of the tumor, the patient underwent resection of the auditory responsive precentral area which resulted in the post-operative expression of a characteristic articulatory disturbance known as apraxia of speech (AOS). The language function of the patient was otherwise preserved and she exhibited intact comprehension of both spoken and written language. The present findings demonstrated that a lesion restricted to the ventral precentral gyrus is sufficient for the expression of AOS and suggest that the auditory-responsive area plays an important role in the execution of fluent speech rather than the comprehension of speech. These findings also confirm that the function of the premotor area is predominantly motor in nature and its sensory responses is more consistent with the "sensory theory of speech production," in which it was proposed that sensory representations are used to guide motor-articulatory processes.

Keywords: TMS; apraxia of speech; mirror neuron; motor theory of speech perception; premotor area.

Figure 1

(A) Preoperative MR image of the patient's brain; the ellipsoid indicates the location of the tumor. CS, central sulcus; PCS, precentral sulcus. (B) Axial section of the preoperative T1-weighted MRI; the arrow indicates the tumor in the left precentral gyrus.

Figure 2

(A) Rendered MR image in which the dots indicate the positions of the electrodes from which responses to the verb generation task were recorded. (B) Positioning of electrodes overlaid on the cortical surface prior to tumor resection; green dots indicate electrodes in the precentral gyrus that recorded auditory responses. (C) Magnified view of a representative time-frequency plot (channel 50). The horizontal axis represents time, the vertical axis represents frequency, and the colors indicate the magnitudes of the response (dB) relative to the baseline period; the purple dotted line indicates the time (0 s) when the noun was presented. (D) Time-frequency plots of the recorded signal in response to the verb generation task with auditory noun presentation. (E) Time-frequency plots of the recorded signal in response to the verb generation task with visual noun presentation. Blank rectangles indicate bad channels.

Figure 3

Power curve in the 60–140 Hz band under auditory (red) and visual (green) conditions. Indicating (upper row) biphasic responses with the auditory-selective response accompanied by the motor response (Channels 30 and 50) and (lower row) monophasic responses with purely motor responses (Channels 28 and 41). The end of stimulus presentation is indicated by the dotted line at 0.65 s while the other dotted line indicates the timing of the “Go” signal at 2.65 s. Gray line indicates mean voice onset time of the subject's response.

Figure 4

(A) Post-operative axial MR image of the resected region (arrow) in a slice most similar to Figure 1B. (B) Resected area (black) superimposed on the cortical surface, with the positioning of the electrodes.