Faculty Bibliography

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. Expected final online publication date for the Annual Review of Neuroscience, Volume 45 is July 2022. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

During conversation, people take turns speaking by rapidly responding to their partners while simultaneously avoiding interruption^1,2. 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 planning^5-9, 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 planning^11-13. 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.

Neural circuits often exhibit sequences of activity, but the contribution of local networks to their generation remains unclear. In the zebra finch, song-related premotor sequences within HVC may result from some combination of local connectivity and long-range thalamic inputs from nucleus uvaeformis (Uva). Because lesions to either structure abolish song, we examine "sleep replay" using high-density recording methods to reconstruct precise song-related events. Replay activity persists after the upstream nucleus interfacialis of the nidopallium is lesioned and slows when HVC is cooled, demonstrating that HVC provides temporal structure for these events. To further gauge the importance of intra-HVC connectivity for shaping network dynamics, we lesion Uva during sleep and find that residual replay sequences could span syllable boundaries, supporting a model in which HVC can propagate sequences throughout the duration of the song. Our results highlight the power of studying offline activity to investigate behaviorally relevant circuit organization.

Establishing a causal link between neural function and behavioral output has remained a challenging problem. Commonly used perturbation techniques enable unprecedented control over intrinsic activity patterns and can effectively identify crucial circuit elements important for specific behaviors. However, these approaches may severely disrupt activity, precluding an investigation into the behavioral relevance of moment-to-moment neural dynamics within a specified brain region. Here we discuss the application of mild focal cooling to slow down intrinsic neural circuit activity while preserving its overall structure. Using network modeling and examples from multiple species, we highlight the power and versatility of focal cooling for understanding how neural dynamics control behavior and argue for its wider adoption within the systems neuroscience community.

INTRODUCTION:Automated text messaging programs have been studied as a treatment tool, but have not been studied as an outreach tool to increase the reach of smoking cessation treatment. AIMS AND METHODS:Two distinct text messaging programs were developed. One was aimed at connecting smokers to quitline phone counseling via text message (Text4Coach [T4C]) and the other was aimed at connecting smokers to a smoking cessation text messaging program (Text&Quit [T&Q]). Adult daily smokers with Medicaid insurance (N = 80) were recruited from the Emergency Department at an urban hospital and randomized to T4C or T&Q. The primary outcome was program reach. RESULTS:Outreach text messages were found to have moderately high uptake, with the majority of participants (63.8%) opting into their assigned tobacco treatment program and younger and female participants more likely to opt in (p < .01). Receipt of the treatment portion of the program differed among the programs with 67.5% of T&Q receiving the treatment program and 27.5% of T4C receiving the program (p < .001). Most participants across both groups replied to at least one message (71.3%) and very few unsubscribed from the service over the 3-week trial. The majority of participants reported overall satisfaction with their program (63.8%), found it helpful for quitting smoking (60.0%) and would recommend the program to a friend (62.5%). Overall, 11 (13.8%) participants reported being abstinent from smoking for the past 7 days at follow-up, with no differences between groups. CONCLUSIONS:Outreach text messages were found to have moderately high reach among Medicaid smokers. Larger trials are needed to evaluate the impact of such programs on helping low-income smokers quit. IMPLICATIONS:Automated text messaging programs have been tested as a treatment tool, but have not been tested as an outreach tool to increase the reach of smoking cessation treatment. This study tests a new way of conducting outreach to smokers in a health system through text messages. It tests the effect of outreach on (1) rates of opting in and (2) successful treatment delivery. Results may inform new models of providing outreach for tobacco treatment in health systems.

OBJECTIVE:Electric cortical stimulation (ECS) has been the gold standard for intraoperative functional mapping in neurosurgery, yet it carries the risk of induced seizures. We assess the safety of focal cortical cooling (CC) as a potential alternative to ECS. METHODS:We reviewed 40 patients (13 with tumor and 27 with mesial temporal lobe epilepsy) who underwent intraoperative CC at the University of Iowa Hospital and Clinics (CC group), of whom 38 underwent ECS preceding CC. Intraoperative and postoperative seizure incidence, postoperative neurologic deficits, and new postoperative radiographic findings were collected to assess CC safety. Fifty-five patients who underwent ECS mapping without CC (ECS-alone group) were reviewed as a control cohort. Another 25 patients who underwent anterior temporal lobectomy (ATL) without CC or ECS (no ECS/no CC-ATL group) were also reviewed to evaluate long-term effects of CC. RESULTS:Seventy-nine brain sites in the CC group were cooled, comprising inferior frontal gyrus (44%), precentral gyrus (39%), postcentral gyrus (6%), subcentral gyrus (4%), and superior temporal gyrus (6%). The incidence of intraoperative seizure(s) was 0% (CC group) and 3.6% (ECS-alone group). The incidence of seizure(s) within the first postoperative week did not significantly differ among CC (7.9%), ECS-alone (9.0%), and no ECS/no CC-ATL groups (12%). There was no significant difference in the incidence of postoperative radiographic change between CC (7.5%) and ECS-alone groups (5.5%). Long-term seizure outcome (Engel I+II) for mesial temporal epilepsy did not differ among CC (80%), ECS-alone (83.3%), and no ECS/no CC-ATL groups (83.3%). CONCLUSIONS:CC when used as an intraoperative mapping technique is safe and may complement ECS.

Sequential activation of neurons has been observed during various behavioral and cognitive processes, but the underlying circuit mechanisms remain poorly understood. Here, we investigate premotor sequences in HVC (proper name) of the adult zebra finch forebrain that are central to the performance of the temporally precise courtship song. We use high-density silicon probes to measure song-related population activity, and we compare these observations with predictions from a range of network models. Our results support a circuit architecture in which heterogeneous delays between sequentially active neurons shape the spatiotemporal patterns of HVC premotor neuron activity. We gauge the impact of several delay sources, and we find the primary contributor to be slow conduction through axonal collaterals within HVC, which typically adds between 1 and 7.5 ms for each link within the sequence. Thus, local axonal "delay lines" can play an important role in determining the dynamical repertoire of neural circuits.

A Quick guide to singing mice.

Like many adaptive behaviors, acoustic communication often requires rapid modification of motor output in response to sensory cues. However, little is known about the sensorimotor transformations that underlie such complex natural behaviors. In this study, we examine vocal exchanges in Alston's singing mouse (Scotinomys teguina). We find that males modify singing behavior during social interactions on a subsecond time course that resembles both traditional sensorimotor tasks and conversational speech. We identify an orofacial motor cortical region and, via a series of perturbation experiments, demonstrate a hierarchical control of vocal production, with the motor cortex influencing the pacing of singing behavior on a moment-by-moment basis, enabling precise vocal interactions. These results suggest a systems-level framework for understanding the sensorimotor transformations that underlie natural social interactions.