Steffen R. Hage

Single neurons in monkey prefrontal cortex encode volitional initiation of vocalizations

Brocas area in the ventrolateral prefrontal cortex (vlPFC) has a crucial role in human volitional speech production; damage to this area causes severe impairment of speech production. Lesions in PFC of monkeys, however, have only mild effects on spontaneous vocal behaviour. Non-human primate vocalizations are thus believed to constitute affective utterances processed by a subcortical network. Here in contrast to this assumption, we show that rhesus monkeys can control their vocalizations in a goal-directed way. During single-cell recordings in the vlPFC of monkeys trained to vocalize in response to visual cues, we find call-related neurons that specifically predict the preparation of instructed vocalizations. The activity of many call-related neurons before vocal output correlates with call parameters of instructed vocalizations. These findings suggest a cardinal role of the monkey homologue of Brocas area in vocal planning and call initiation, a putative phylogenetic precursor in non-human primates for speech control in linguistic humans.

Dual Neural Network Model for the Evolution of Speech and Language

Explaining the evolution of speech and language poses one of the biggest challenges in biology. We propose a dual network model that posits a volitional articulatory motor network (VAMN) originating in the prefrontal cortex (PFC; including Brocas area) that cognitively controls vocal output of a phylogenetically conserved primary vocal motor network (PVMN) situated in subcortical structures. By comparing the connections between these two systems in human and nonhuman primate brains, we identify crucial biological preadaptations in monkeys for the emergence of a language system in humans. This model of language evolution explains the exclusiveness of non-verbal communication sounds (e.g., cries) in infants with an immature PFC, as well as the observed emergence of non-linguistic vocalizations in adults after frontal lobe pathologies.

Limiting parental feedback disrupts vocal development in marmoset monkeys

Vocalizations of human infants undergo dramatic changes across the first year by becoming increasingly mature and speech-like. Human vocal development is partially dependent on learning by imitation through social feedback between infants and caregivers. Recent studies revealed similar developmental processes being influenced by parental feedback in marmoset monkeys for apparently innate vocalizations. Marmosets produce infant-specific vocalizations that disappear after the first postnatal months. However, it is yet unclear whether parental feedback is an obligate requirement for proper vocal development. Using quantitative measures to compare call parameters and vocal sequence structure we show that, in contrast to normally raised marmosets, marmosets that were separated from parents after the third postnatal month still produced infant-specific vocal behaviour at subadult stages. These findings suggest a significant role of social feedback on primate vocal development until the subadult stages and further show that marmoset monkeys are a compelling model system for early human vocal development.

Developmental changes of cognitive vocal control in monkeys.

ABSTRACT The evolutionary origins of human language are obscured by the scarcity of essential linguistic characteristics in non-human primate communication systems. Volitional control of vocal utterances is one such indispensable feature of language. We investigated the ability of two monkeys to volitionally utter species-specific calls over many years. Both monkeys reliably vocalized on command during juvenile periods, but discontinued this controlled vocal behavior in adulthood. This emerging disability was confined to volitional vocal production, as the monkeys continued to vocalize spontaneously. In addition, they continued to use hand movements as instructed responses during adulthood. This greater vocal flexibility of monkeys early in ontogeny supports the neoteny hypothesis in human evolution. This suggests that linguistic capabilities were enabled via an expansion of the juvenile period during the development of humans. Highlighted Article: Monkeys reliably vocalize on command during juvenile periods, but discontinue this behavior in adulthood. This greater vocal flexibility of monkeys early in ontogeny supports the neoteny hypothesis in human evolution.

Behavioural and neurobiological implications of linear and non-linear features in larynx phonations of horseshoe bats

Mammalian vocalizations exhibit large variations in their spectrotemporal features, although it is still largely unknown which result from intrinsic biomechanical properties of the larynx and which are under direct neuromuscular control. Here we show that mere changes in laryngeal air flow yield several non-linear effects on sound production, in an isolated larynx preparation from horseshoe bats. Most notably, there are sudden jumps between two frequency bands used for either echolocation or communication in natural vocalizations. These jumps resemble changes in “registers” as in yodelling. In contrast, simulated contractions of the main larynx muscle produce linear frequency changes, but are limited to echolocation or communication frequencies. Only by combining non-linear and linear properties can this larynx therefore produce sounds covering the entire frequency range of natural calls. This may give behavioural meaning to yodelling-like vocal behaviour and reshape our thinking about how the brain controls the multitude of spectral vocal features in mammals.

Temporal vocal features suggest different call-pattern generating mechanisms in mice and bats

BackgroundMice produce ultrasonic vocalizations in various inter-individual encounters and with high call rates. However, it is so far virtually unknown how these vocal patterns are generated. On the one hand, these vocal patterns could be embedded into the normal respiratory cycle, as happens in bats and other mammals that produce similar call rates and frequencies. On the other, mice could possess distinct vocal pattern generating systems that are capable of modulating the respiratory cycle, which is what happens in non-human and human primates. In the present study, we investigated the temporal call patterns of two different mammalian species, bats and mice, in order to differentiate between these two possibilities for mouse vocalizations. Our primary focus was on comparing the mechanisms for the production of rapid, successive ultrasound calls of comparable frequency ranges in the two species.ResultsWe analyzed the temporal call pattern characteristics of mice, and we compared these characteristics to those of ultrasonic echolocation calls produced by horseshoe bats. We measured the distributions of call durations, call intervals, and inter-call intervals in the two species. In the bat, and consistent with previous studies, we found that call duration was independent of corresponding call intervals, and that it was negatively correlated with the corresponding inter-call interval. This indicates that echolocation call production mechanisms in the bat are highly correlated with the respiratory cycle. In contrast, call intervals in the mouse were directly correlated with call duration. Importantly, call duration was not, or was only slightly, correlated with inter-call intervals, consistent with the idea that vocal production in the mouse is largely independent of the respiratory cycle.ConclusionsOur findings suggest that ultrasonic vocalizations in mice are produced by call-pattern generating mechanisms that seem to be similar to those that have been found in primates. This is in contrast to the production mechanisms of ultrasonic echolocation calls in horseshoe bats. These results are particularly interesting, especially since mouse vocalizations have recently attracted increased attention as potential indicators for the degree of progression of several disease patterns in mouse models for neurodegenerative and neurodevelopmental disorders of humans.

Functional Specialization of the Primate Frontal Lobe during Cognitive Control of Vocalizations

Cognitive vocal control is indispensable for human language. Frontal lobe areas are involved in initiating purposeful vocalizations, but their functions remain elusive. We explored the respective roles of frontal lobe areas in initiating volitional vocalizations. Macaques were trained to vocalize in response to visual cues. Recordings from the ventrolateral prefrontal cortex (vlPFC), the anterior cingulate cortex (ACC), and the pre-supplementary motor area (preSMA) revealed single-neuron and population activity differences. Pre-vocal activity appeared first after the go cue in vlPFC, showing onset activity that was tightly linked to vocal reaction times. However, pre-vocal ACC onset activity was not indicative of call timing; instead, ramping activity reaching threshold values betrayed call onset. Neurons in preSMA showed weakest correlation with volitional call initiation and timing. These results suggest that vlPFC encodes the decision to produce volitional calls, whereas downstream ACC represents a motivational preparatory signal, followed by a general motor priming signal in preSMA.

Phylogenetic reorganization of the basal ganglia: A necessary, but not the only, bridge over a primate Rubicon of acoustic communication

In this response to commentaries, we revisit the two main arguments of our target article. Based on data drawn from a variety of research areas – vocal behavior in nonhuman primates, speech physiology and pathology, neurobiology of basal ganglia functions, motor skill learning, paleoanthropological concepts – the target article, first, suggests a two-stage model of the evolution of the crucial motor prerequisites of spoken language within the hominin lineage: (1) monosynaptic refinement of the projections of motor cortex to brainstem nuclei steering laryngeal muscles, and (2) subsequent “vocal-laryngeal elaboration” of cortico-basal ganglia circuits, driven by human-specific FOXP2 mutations. Second, as concerns the ontogenetic development of verbal communication, age-dependent interactions between the basal ganglia and their cortical targets are assumed to contribute to the time course of the acquisition of articulate speech. Whereas such a phylogenetic reorganization of cortico-striatal circuits must be considered a necessary prerequisite for ontogenetic speech acquisition, the 30 commentaries – addressing the whole range of data sources referred to – point at several further aspects of acoustic communication which have to be added to or integrated with the presented model. For example, the relationships between vocal tract movement sequencing – the focus of the target article – and rhythmical structures of movement organization, the connections between speech motor control and the central-auditory and central-visual systems, the impact of social factors upon the development of vocal behavior (in nonhuman primates and in our species), and the interactions of ontogenetic speech acquisition – based upon FOXP2-driven structural changes at the level of the basal ganglia – with preceding subvocal stages of acoustic communication as well as higher-order (cognitive) dimensions of phonological development. Most importantly, thus, several promising future research directions unfold from these contributions – accessible to clinical studies and functional imaging in our species as well as experimental investigations in nonhuman primates.

Dual neural network model of speech and language evolution: new insights on flexibility of vocal production systems and involvement of frontal cortex

Human speech vastly outperforms primate vocal behavior in scope and flexibility making the elucidation of speech evolution one of biologys biggest challenges. A proposed dual-network model including a volitional articulatory motor network originating in the prefrontal cortex that is capable of cognitively controlling vocal output of a phylogenetically conserved primary vocal motor network attempts to bridge this gap. By comparing neuronal networks in human and non-human brains, crucial biological preadaptations are found in monkeys for the emergence of a speech system in humans. This model can explain behavioral evidence for vocal flexibility in cognitive tasks as well as during vocal development in monkeys as intermediate steps in the continuous evolution of speech in the primate lineage.

The Lombard Effect: From Acoustics to Neural Mechanisms

Understanding the neural underpinnings of vocal-motor control in humans and other animals remains a major challenge in neurobiology. The Lombard effect - a rise in call amplitude in response to background noise - has been demonstrated in a wide range of vertebrates. Here, we review both behavioral and neurophysiological data and propose that the Lombard effect is driven by a subcortical neural network, which can be modulated by cortical processes. The proposed framework offers mechanistic explanations for two fundamental features of the Lombard effect: its widespread taxonomic distribution across the vertebrate phylogenetic tree and the widely observed variations in compensation magnitude. We highlight the Lombard effect as a model behavioral paradigm for unraveling some of the neural underpinnings of audiovocal integration.