A Theoretical Framework for Human and Nonhuman Vocal Interaction.

Vocal communication is a critical feature of social interaction across species; however, the relation between such behavior in humans and nonhumans remains unclear. To enable comparative investigation of this topic, we review the literature pertinent to interactive language use and identify the superset of cognitive operations involved in generating communicative action. We posit these functions comprise three intersecting multistep pathways: (a) the Content Pathway, which selects the movements constituting a response; (b) the Timing Pathway, which temporally structures responses; and (c) the Affect Pathway, which modulates response parameters according to internal state. These processing streams form the basis of the Convergent Pathways for Interaction framework, which provides a conceptual model for investigating the cognitive and neural computations underlying vocal communication across species.

A speech planning network for interactive language use.

During conversation, people take turns speaking by rapidly responding to their partners while simultaneously avoiding interruption1,2. Such interactions display a remarkable degree of coordination, as gaps between turns are typically about 200 milliseconds3-approximately the duration of an eyeblink4. These latencies are considerably shorter than those observed in simple word-production tasks, which indicates that speakers often plan their responses while listening to their partners2. Although a distributed network of brain regions has been implicated in speech planning5-9, the neural dynamics underlying the specific preparatory processes that enable rapid turn-taking are poorly understood. Here we use intracranial electrocorticography to precisely measure neural activity as participants perform interactive tasks, and we observe a functionally and anatomically distinct class of planning-related cortical dynamics. We localize these responses to a frontotemporal circuit centred on the language-critical caudal inferior frontal cortex10 (Broca's region) and the caudal middle frontal gyrus-a region not normally implicated in speech planning11-13. Using a series of motor tasks, we then show that this planning network is more active when preparing speech as opposed to non-linguistic actions. Finally, we delineate planning-related circuitry during natural conversation that is nearly identical to the network mapped with our interactive tasks, and we find this circuit to be most active before participant speech during unconstrained turn-taking. Therefore, we have identified a speech planning network that is central to natural language generation during social interaction.

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

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 operations1,5,6 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 errors9,13,20,21 but not gross articulatory deficits, which instead resulted from DES of structures involved in motor control8,13,20,22 (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.

A frontal cortical network is critical for language planning during spoken interaction.

Many brain areas exhibit activity correlated with language planning, but the impact of these dynamics on spoken interaction remains unclear. Here we use direct electrical stimulation to transiently perturb cortical function in neurosurgical patient-volunteers performing a question-answer task. Stimulating structures involved in speech motor function evoked diverse articulatory deficits, while perturbations of caudal inferior and middle frontal gyri - which exhibit preparatory activity during conversational turn-taking - led to response errors. Perturbation of the same planning-related frontal regions slowed inter-speaker timing, while faster responses could result from stimulation of sites located in other areas. Taken together, these findings further indicate that caudal inferior and middle frontal gyri constitute a critical planning network essential for interactive language use.

The temporal organization of mouse ultrasonic vocalizations.

House mice, like many tetrapods, produce multielement calls consisting of individual vocalizations repeated in rhythmic series. In this study, we examine the multielement ultrasonic vocalizations (USVs) of adult male C57Bl/6J mice and specifically assess their temporal properties and organization. We found that male mice produce two classes of USVs which display unique temporal features and arise from discrete respiratory patterns. We also observed that nearly all USVs were produced in repetitive series exhibiting a hierarchical organization and a stereotyped rhythmic structure. Furthermore, series rhythmicity alone was determined to be sufficient for the mathematical discrimination of USVs produced by adult males, adult females, and pups, underscoring the known importance of call timing in USV perception. Finally, the gross spectrotemporal features of male USVs were found to develop continuously from birth and stabilize by P50, suggesting that USV production in infants and adults relies on common biological mechanisms. In conclusion, we demonstrate that the temporal organization of multielement mouse USVs is both stable and informative, and we propose that call timing be explicitly assessed when examining mouse USV production. Furthermore, this is the first report of putative USV classes arising from distinct articulatory patterns in mice, and is the first to empirically define multielement USV series and provide a detailed description of their temporal structure and development. This study therefore represents an important point of reference for the analysis of mouse USVs, a commonly used metric of social behavior in mouse models of human disease, and furthers the understanding of vocalization production in an accessible mammalian species.

Knockout of Foxp2 disrupts vocal development in mice.

The FOXP2 gene is important for the development of proper speech motor control in humans. However, the role of the gene in general vocal behavior in other mammals, including mice, is unclear. Here, we track the vocal development of Foxp2 heterozygous knockout (Foxp2+/-) mice and their wildtype (WT) littermates from juvenile to adult ages, and observe severe abnormalities in the courtship song of Foxp2+/- mice. In comparison to their WT littermates, Foxp2+/- mice vocalized less, produced shorter syllable sequences, and possessed an abnormal syllable inventory. In addition, Foxp2+/- song also exhibited irregular rhythmic structure, and its development did not follow the consistent trajectories observed in WT vocalizations. These results demonstrate that the Foxp2 gene is critical for normal vocal behavior in juvenile and adult mice, and that Foxp2 mutant mice may provide a tractable model system for the study of the gene's role in general vocal motor control.