Stimulation of caudal inferior and middle frontal gyri disrupts planning during spoken interaction

Abstract

Turn-taking is a central feature of conversation across languages and cultures.^1,2,3,4 This key social behavior requires numerous sensorimotor and cognitive operations^1,5,6 that can be organized into three general phases: comprehension of a partner's turn, preparation of a speaker's own turn, and execution of that turn. Using intracranial electrocorticography, we recently demonstrated that neural activity related to these phases is functionally distinct during turn-taking.⁷ In particular, networks active during the perceptual and articulatory stages of turn-taking consisted of structures known to be important for speech-related sensory and motor processing,^{8,9,10,11,12,13,14,15,16,17} while putative planning dynamics were most regularly observed in the caudal inferior frontal gyrus (cIFG) and the middle frontal gyrus (cMFG). To test if these structures are necessary for planning during spoken interaction, we used direct electrical stimulation (DES) to transiently perturb cortical function in neurosurgical patient-volunteers performing a question-answer task.^7,18,19 We found that stimulating the cIFG and cMFG led to various response errors^9,13,20,21 but not gross articulatory deficits, which instead resulted from DES of structures involved in motor control^8,13,20,22 (e.g., the precentral gyrus). Furthermore, perturbation of the cIFG and cMFG delayed inter-speaker timing-consistent with slowed planning-while faster responses could result from stimulation of sites located in other areas. Taken together, our findings suggest that the cIFG and cMFG contain critical preparatory circuits that are relevant for interactive language use.

Keywords: cognition; cortex; interaction; language; neurosurgery; planning; speech; stimulation.

Figure 1.. DES evokes motor deficits.

(A) Example critical information (CI) questions where the CI is presented early (top) or late (bottom) with behavioral phases indicated. (B) Left lateral cortical surface of participant 494L with two stimulation sites indicated. (C) Example control trial (left) and trial where stimulation of the posterior site in (B) resulted in articulatory disruption (right); spectrograms of participant response with formant frequencies and envelope amplitude indicated (bottom). (D) Schematics of all trials where the anterior site in (B) was stimulated (left) with latencies between stimulation and speech onset shown at right. See also Figure S1. (E) Canonical cortical surface depicting all sites across participants where stimulation evoked motor deficits; all 6 stimulation sites within non-surface structures did not display motor disruptions (Table S2). The location of precentral and postcentral gyri is approximated in light red, and the regions of caudal inferior and middle frontal gyri displaying neural activity related to language planning are approximated in light blue.

Figure 2.. DES can elicit qualitative increases in the rate of putative planning-related errors.

(A) Preoperative magnetic resonance images depicting the stimulation site within the Basal Temporal Language Area (BTLA). At right, example control trial (top) and trial where BTLA stimulation resulted in semantic paraphasia (bottom); spectrograms and envelope amplitude of example responses are also presented (middle). (B-C) Example trials from sites where stimulation induced anomia (B) and hesitations (C); site locations indicated on participant cortical surfaces at left. (D) Cumulative distribution functions of error counts in control and stimulated trials across sites; inset scatterplots depict error rates. (E) Bar graph depicting the percentage of sites across participants where stimulation increased rates of one, two, or three error types (i.e., semantic paraphasia, anomia, or hesitations; in blue) or did not affect error rates (in white); the location of each site is shown on canonical cortical surfaces at right and its effect on error rates is indicated with colored circles. Arrow points to site displaying stimulation-induced neologisms. The location of precentral and postcentral gyri is approximated in light red, and the regions of caudal inferior and middle frontal gyri displaying neural activity related to language planning7 are approximated in light blue. Stimulation of sites in non-surface structures led to increases in either three error types (n = 1; BTLA site), one error type (n = 3), or no error types (n = 2) (Table S2).

Figure 3.. DES-induced modulations of inter-turn gap duration suggest distinct planning loci.

(A) Example control trial (top left) and trial where the Basal Temporal Language Area (BTLA; see Figure 2A) was stimulated (bottom left) with inter-turn gap durations indicated; spectrograms of participant response with envelope amplitude overlaid (right). (B) All trials related to stimulation of the site in (A) sorted by gap duration. (C-E) Cumulative distribution functions of gap duration for example sites where stimulation induced longer gaps (C), shorter gaps (D), or no statistical difference in gap duration (E); site location indicated on participant cortical surfaces at top. (F-H) The error rates in control and stimulated trials for all sites where stimulation resulted in longer gaps (F), shorter gaps (G), or no effect on gap duration (H). For (F), the site which displayed stimulation-induced perceptual deficits (see Figure S2) is indicated with an arrow and was excluded from analyses of anomia. (I) Median and interquartile range of gap duration for all sites where stimulation significantly affected this measure (left); sites where DES induced shorter gaps on late CI trials only indicated with asterisks. Participant and site number indicated in leftmost column (i.e., participant #, site #). At right, canonical cortical surfaces depicting the effect of stimulation on gap duration in all sites across participants; stimulation of sites in non-surface structures either lengthened gaps (n = 2; i.e., BTLA and posterior cingulate gyrus) or did not affect gap duration (n = 4) (Table S2). The location of precentral and postcentral gyri is approximated in light red, and the regions of caudal inferior and middle frontal gyri displaying neural activity related to language planning7 are approximated in light blue. The site which displayed stimulation-induced perceptual deficits (see Figure S2) is indicated with an arrow. See also Figure S3.