Language appears to be the most complex system of animal communication described to date. However, its precursors were present in the communication of our evolutionary ancestors and are likely shared by our modern ape cousins.  All great apes, including humans, employ a rich repertoire of vocalizations, facial expressions, and gestures. Great ape gestural repertoires are particularly elaborate, with ape species employing over 80 different gesture types intentionally: that is towards a recipient with a specific goal in mind. Intentional usage allows us to ask not only what information is encoded in ape gestures, but what do apes mean when they use them. I will discuss recent research on ape gesture, on how we approach the question of decoding meaning, and how with new methods we are starting to integrate long overlooked aspects of ape gesture such as group and individual variation, and expression and emotion into our study of these signals.

To communicate effectively, two individuals must take turns to prevent overlap in their signals. How does the nervous system coordinate vocalizations between two individuals? Female and male plain-tailed wrens sing a duet in which they alternate syllable production so rapidly and precisely it sounds as if a single bird is singing. I will talk about experiments that examine the interaction between sensory cues and motor activity, using behavioral manipulations and neurophysiological recordings from pairs of awake, duetting wrens. I will show evidence that auditory cues link the brains of the wrens by modulating motor circuits.

Maternal care is profoundly important for mammalian survival, and in many species requires the contribution of non-biological parents, or alloparents. In the absence of partum and post-partum related hormonal changes, alloparents acquire maternal skills from experience, by yet unknown mechanisms. One critical molecular signal for maternal behavior is oxytocin, a hormone centrally released by hypothalamic paraventricular nucleus (PVN). Do experiences that induce maternal behavior act by engaging PVN oxytocin neurons? To answer this, we used virgin female mice, animals that in the wild live in colonies with experienced mothers and their pups, helping with pup care. We replicated this setup in the lab, and we continuously monitored homecage behavior of virgin mice co-housed for days with a mother and litter, synchronized with recordings from virgin PVN cells, including from oxytocin neurons. Mothers engaged virgins in maternal care in part by shepherding virgins towards the nest, ensuring their proximity to pups, and in part by self-generating pup retrieval episodes, demonstrating maternal behavior to virgins. The frequency of shepherding and of dam retrievals correlates with virgin's subsequent ability to retrieve pups, a quintessential mouse maternal skill. These social interactions activated virgin PVN and gated behaviorally-relevant cortical plasticity for pup vocalizations. Thus, rodents can acquire maternal behavior by social transmission, and our results describe a mechanism for adapting brains of adult caregivers to infant needs via endogenous oxytocin.

Mammalian babies are “sensory traps” for parents. Various sensory cues from the newborn are tremendously efficient in triggering parental responses in caregivers. We recently showed that core aspects of maternal behavior such as pup retrieval in response to infant vocalizations rely on active learning of auditory cues from pups facilitated by the neurohormone oxytocin (OT). Release of OT from the hypothalamus might thus help induce recognition of different infant cues but it is unknown what sensory stimuli can activate OT neurons. I performed unprecedented in vivo whole-cell and cell-attached recordings from optically-identified OT neurons in awake dams. I found that OT neurons, but not other hypothalamic cells, increased their firing rate after playback of pup distress vocalizations. Using anatomical tracing approaches and channelrhodopsin-assisted circuit mapping, I identified the projections and brain areas (including inferior colliculus, auditory cortex, and posterior intralaminar thalamus) relaying auditory information about social sounds to OT neurons. In hypothalamic brain slices, when optogenetically stimulating thalamic afferences to mimic high-frequency thalamic discharge, observed in vivo during pup calls playback, I found that thalamic activity led to long-term depression of synaptic inhibition in OT neurons. This was mediated by postsynaptic NMDARs-induced internalization of GABAARs. Therefore, persistent activation of OT neurons following pup calls in vivo is likely mediated by disinhibition. This gain modulation of OT neurons by infant cries, may be important for sustaining motivation. Using a genetically-encoded OT sensor, I demonstrated that pup calls were efficient in triggering OT release in downstream motivational areas. When thalamus projections to hypothalamus were inhibited with chemogenetics, dams exhibited longer latencies to retrieve crying pups, suggesting that the thalamus-hypothalamus noncanonical auditory pathway may be a specific circuit for the detection of social sounds, important for disinhibiting OT neurons, gating OT release in downstream brain areas, and speeding up maternal behavior.

The evolution of speech is considered to be one of the hardest problems in science. Studies of the communicative abilities of our closest living relatives, the nonhuman primates, aim to contribute to a better understanding of the emergence of this uniquely human capability. Following a brief introduction over the key building blocks that make up the human speech faculty, I will focus on the question of meaning in nonhuman primate vocalizations. While nonhuman primate calls may be highly context specific, thus giving rise to the notion of ‘referentiality’, comparisons across closely related species suggest that this specificity is evolved rather than learned. Yet, as in humans, the structure of calls varies with arousal and affective state, and there is some evidence for effects of sensory-motor integration in vocal production. Thus, the vocal production of nonhuman primates bears little resemblance to the symbolic and combinatorial features of human speech, while basic production mechanisms are shared. Listeners, in contrast, are able learning the meaning of new sounds. A recent study using artificial predator shows that this learning may be extremely rapid. Furthermore, listeners are able to integrate information from multiple sources to make adaptive decisions, which renders the vocal communication system as a whole relatively flexible and powerful. In conclusion, constraints at the side of vocal production, including limits in social cognition and motivation to share experiences, rather than constraints at the side of the recipient explain the differences in communicative abilities between humans and other animals.

Attending to mistakes while practicing alone provides opportunities for learning but self-evaluation during audience-directed performance could distract from ongoing execution. It remains unknown how animals switch between practice and performance modes, and how evaluation systems process errors across distinct performance contexts. We recorded from striatal-projecting dopamine (DA) neurons as male songbirds transitioned from singing alone to singing female-directed courtship song. In the presence of the female, singing-related performance error signals were reduced or gated off and DA neurons were instead phasically activated by female vocalizations. Mesostriatal DA neurons can thus dynamically change their tuning with changes in social context.

During conversations we rapidly switch between listening and speaking which often requires withholding or delaying our speech in order to hear others and avoid overlapping. This capacity for vocal turn-taking is exhibited by non-linguistic species as well, however the neural circuit mechanisms that enable us to regulate the precise timing of our vocalizations during interactions are unknown. We aim to identify the neural mechanisms underlying the coordination of vocal interactions. Therefore, we paired zebra finches with a vocal robot (1Hz call playback) and measured the bird’s call response times. We found that individual birds called with a stereotyped delay in respect to the robot call. Pharmacological inactivation of the premotor nucleus HVC revealed its necessity for the temporal coordination of calls. We further investigated the contributing neural activity within HVC by performing intracellular recordings from premotor neurons and inhibitory interneurons in calling zebra finches. We found that inhibition is preceding excitation before and during call onset. To test whether inhibition guides call timing we pharmacologically limited the impact of inhibition on premotor neurons. As a result zebra finches converged on a similar delay time i.e. birds called more rapidly after the vocal robot call suggesting that HVC inhibitory interneurons regulate the coordination of social contact calls. In addition, we aim to investigate the vocal turn-taking capabilities of the common nightingale. Male nightingales learn over 100 different song motifs which are being used in order to attract mates or defend territories. Previously, it has been shown that nightingales counter-sing with each other following a similar temporal structure to human vocal turn-taking. These animals are also able to spontaneously imitate a motif of another nightingale. The neural mechanisms underlying this behaviour are not yet understood. In my lab, we further probe the capabilities of these animals in order to access the dynamic range of their vocal turn taking flexibility.