Biology subjects

Ghazanfar, A. A.

Publications and source records attributed to Ghazanfar, A. A..

6 recordsLinked to original sources

bioRxiv2024

Altricial brains and the evolution of infant vocal learning

Human infant vocal development is strongly influenced by interactions with caregivers who reinforce more speech-like sounds. This trajectory of vocal development in humans is radically different from those of our close phylogenetic relatives, Old World monkeys and apes. In these primates most closely related to humans on the evolutionary tree, social feedback plays no significant role in their vocal development. Oddly, infant marmoset monkeys, a more distantly related New World primate, do exhibit socially guided vocal learning. To explore what developmental mechanism could have evolved to account for these behavioral differences, we hypothesized that the evolution of human and marmoset vocal learning in early infancy in both species is because they are born neurally altricial relative to other primate and in a cooperative breeding social environment. Our analysis found that, indeed, human and marmoset brain are growing faster at birth when compared with chimpanzees and rhesus macaques, making them altricial relative to these primates. We formalized our hypothesis using a logistic growth model showing that the maturation of a system dependent on the rate of brain growth and the amount of social stimuli benefits from an altricial brain and a cooperative breeding environment. Our data suggest that in primates, the evolution of socially guided vocal learning during early infancy in humans and marmosets was afforded by infants with a relatively altricial brain and behavior, sustained and stimulated by cooperative breeding environments. Significance statementHumans rely on social feedback from caregivers to learn how to produce species-typical sounds, whereas other primates like macaque monkeys or chimpanzees do not. What accounts for this difference in developmental strategies? We tested the hypothesis that being born with a more immature (thus more plastic) brain may be the reason by using marmoset monkeys. This species is more distantly related to humans but exhibit the same type of vocal learning and who have a similar socially rich infant care environment. We found that, indeed, human and marmoset brain are growing faster at birth when compared with chimpanzees and rhesus macaques, making them altricial relative to these primates and this explains their similar vocal developmental strategies.

neuroscience↗

bioRxiv2023

Active Sampling in Primate Vocal Interactions

Active sensing is a behavioral strategy for exploring the environment. In this study, we show that contact vocal behaviors can be an active sensing mechanism that uses sampling to gain information about the social environment, in particular, the vocal behavior of others. With a focus on the real-time vocal interactions of marmoset monkeys, we contrast active sampling to a vocal accommodation framework in which vocalizations are adjusted simply to maximize responses. We conducted simulations of a vocal accommodation and an active sampling policy and compared them with real vocal exchange data. Our findings support active sampling as the best model for marmoset monkey vocal exchanges. In some cases, the active sampling model was even able to predict the distribution of vocal durations for individuals. These results suggest a new function for primate vocal interactions in which they are used by animals to seek information from social environments. SignificanceWe found that marmoset monkeys use vocal exchanges with conspecifics in the same way that bats and electric fish use their self-generated signals: to sample the information space. The difference is that, while bats, electric fish and other echolocating animals emit signals and then interpret that signals reflection, for vocalizing marmoset monkeys the "reflection" is the vocal response from conspecifics. We show that marmosets produce variable vocalizations as a means to sample the acoustic space in which they can elicit a conspecific response. They are actively sampling--learning about their dyadic partner like a bat learns about its prey.

animal behavior and cognition↗

bioRxiv2022

Prenatal development of neonatal vocalizations

Human and non-human primates produce rhythmical sounds as soon as they are born. These early vocalizations are important for soliciting the attention of caregivers. How they develop, remains a mystery. The orofacial movements necessary for producing these vocalizations have distinct spatiotemporal signatures. Therefore, their development could potentially be tracked over the course of prenatal life. We densely and longitudinally sampled fetal head and orofacial movements in marmoset monkeys using ultrasound imaging. We show that orofacial movements necessary for producing rhythmical vocalizations differentiate from a larger movement pattern that includes the entire head. We also show that signature features of marmoset infant contact calls emerge prenatally as a distinct pattern of orofacial movements. Our results establish that aspects of the sensorimotor development necessary for vocalizing occur prenatally, even before the production of sound.

neuroscience↗

bioRxiv2021

Arousal elevation drives the development of oscillatory vocal output

Adult behaviors, such as vocal production, often exhibit temporal regularity. In contrast, their immature forms are more irregular. We ask whether the coupling of motor behaviors with arousal changes give rise to temporal regularity. Do they drive the transition from variable to regular motor output over the course of development? We used marmoset monkey vocal production to explore this putative influence of arousal on the nonlinear changes in their developing vocal output patterns. Based on a detailed analysis of vocal and arousal dynamics in marmosets, we put forth a general model incorporating arousal and auditory-feedback loops for spontaneous vocal production. Using this model, we show that a stable oscillation can emerge as the baseline arousal increases, predicting the transition from stochastic to periodic oscillations observed during marmoset vocal development. We further provide a solution for how this model can explain vocal development as the joint consequence of energetic growth and social feedback. Together, we put forth a plausible mechanism for the development of arousal-mediated adaptive behavior.

neuroscience↗

bioRxiv2021

Active neural coordination of motor behaviors with internal states

The brain continuously coordinates skeletomuscular movements with internal physiological states like arousal, but how is this coordination achieved? One possibility is that brain simply reacts to changes in external and/or internal signals. Another possibility is that it is actively coordinating both external and internal activities. We used functional ultrasound imaging to capture a large medial section of the brain, including multiple cortical and subcortical areas, in marmoset monkeys while monitoring their spontaneous movements and cardiac activity. By analyzing the causal ordering of these different time-series, we found that information flowing from the brain to movements and heart rate fluctuations were significantly greater than in the opposite direction. The brain areas involved in this external versus internal coordination were spatially distinct but also extensively interconnected. Temporally, the brain alternated between network states for this regulation. These findings suggest that the brains dynamics actively and efficiently coordinate motor behavior with internal physiology.

neuroscience↗

bioRxiv2021

Social-vocal brain networks in a non-human primate

During social interactions, individuals influence each other to coordinate their actions. Vocal communication is an exceptionally efficient way to exert such influence. Where and how social interactions are dynamically modulated in the brain is unknown. We used functional ultrasound imaging in marmoset monkeys - a highly vocal species - to investigate the dynamics of medial social brain areas in vocal perception, production, and audio-vocal interaction. We found that the activity of a distributed network of subcortical and cortical regions distinguishes calls associated with different social contexts. This same brain network showed different dynamics during externally and internally driven vocalizations. These findings suggest the existence of a social-vocal brain network in medial cortical and subcortical areas that is fundamental in social communication. One Sentence SummaryA network of medial subcortical and cortical brain areas gate social communication in primates.

neuroscience↗