From Rainforest Calls to Human Conversations: Marmosets and the Neuroscience of Vocal Communication

Electrophysiological investigations of marmoset area 32 begin to unveil the region’s contribution to vocalization processing, potentially shedding light on the evolution of our own communication abilities.
From Rainforest Calls to Human Conversations: Marmosets and the Neuroscience of Vocal Communication
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From morning greetings to evening conversations, vocal communication is a daily behaviour that we often take for granted. In truth, our ability to communicate through speech enables us to do remarkable things, such as share ideas, tell stories, and plan for the future. Can you imagine what our lives would look like if we had not developed this ability? 

The loss of vocal communication is devastating. I may know this better than most because in my teen years I suffered a series of intense sports-related concussions that resulted in aphasia, the partial loss of language abilities. The best way I can describe those excruciating months is that I was in a zombie-like state, existing mindlessly, able to perform life-sustaining functions with ease but completely unable to form coherent thought, thereby diminishing all forms of communication to surface-level expression of needs. Fortunately, I eventually made a full recovery, without which this article would have been nothing more than a page splattered with disjointed words. 

Upon my recovery, I was struck by the immense power and importance of vocal communication in our lives, as well as its fragility. This experience is what inspired me to pursue a career in neuroscience. Vocal communication is one of our most sophisticated cognitive abilities, requiring the precise coordination of many cortical and subcortical brain regions, as well as articulatory and respiratory muscles. Given this complexity, it is perhaps unsurprising that we do not fully understand the neural mechanisms underlying vocal communication. Primary reasons for this are that it is notoriously difficult to study intricate neural dynamics in humans due to our limitation to mostly non-invasive techniques, and that few non-human animal models exhibit complex vocal communication behaviors comparable to those of humans. 

The common marmoset (Callithrix jacchus) is a model animal that allows us to address, at least in part, these limitations. This small primate has recently gained traction as a model animal in neuroscience due to its small size, short reproductive cycle, and evolutionary similarity to humans (compared to other common neuroscientific models like rodents and birds). Luckily for us, marmosets are also highly social and vocal, relying heavily on complex vocalizations to communicate with their peers among the dense foliage of the Amazon rainforest. Notable examples highlighting the complexity of this behaviour include conversation-like vocal turn-taking (Takahashi et al., 2013), and the recently revealed use of distinct “names” for their conspecifics (Oren et al., 2024)

The year before I joined Dr. Stefan Everling’s lab at Western University, he began to investigate the neural correlates of vocal communication in marmosets. To lay the groundwork, his group conducted ultra-high field, awake fMRI on marmosets while they listened to recorded marmoset vocalizations. This revealed a network of regions involved in vocalization processing (Jafari et al., 2023). The activation found in many areas was expected based on similar studies in humans. One intriguing finding was the activation of a particular medial prefrontal region, area 32. This brain region has extensive connections with high-level auditory areas, but its specific role in vocalization processing is as yet poorly understood, in part because of a lack of studies investigating its circuit dynamics at the single-neuron level. Thus, my doctoral project was born: electrophysiologically investigating the contribution of area 32 to vocal communication. 

As a first step, we set out to determine the responses of area 32 neurons to vocalizations and other sounds. We used extremely fine ultra-high density Neuropixels electrodes to record simultaneously the activity of many neurons in area 32 of awake marmosets while they were played a small suite of auditory stimuli that included marmoset vocalizations. Our paper presents some of the first evidence that the neurons in area 32 respond to sounds and differentiate between sounds in some way. Intriguingly, many neurons preferred the marmoset vocalization stimuli, supporting the idea that area 32 is involved in vocal communication. To our surprise, the neurons also responded strongly to another non-marmoset, but biologically-relevant sound, the flapping of bird wings.

To unpack our findings, it is important to understand the context in which area 32 functions. Medial prefrontal cortex is generally involved in higher-order cognitive processes, such as decision-making, emotional regulation, and perspective-taking. It contributes to one’s everyday life by integrating cognitive and emotional information in order to inform and regulate subsequent behaviour. For example, when viewing the “Behind the Paper” website, your brain took in and processed a variety of information and feelings. As you scanned the long list of posts, you simultaneously assessed your level of personal interest in each topic, considered the relevance of each post to your own work, weighed the amount of time available in your day for perusing the website, regulated potential feelings of anxiety caused by the overwhelming number of options, and eventually came to a decision to select this particular post. It’s likely that your own area 32 played a key role in quickly integrating these diverse factors to lead to a thoughtful and contextually relevant decision regarding which post to read.

Taking a broad view of area 32 and combining it with our current findings, we propose that it may act to facilitate the processing of behaviourally relevant sounds via communication with other brain regions. One striking aspect of the response dynamics of these neurons was that very early excitatory and sound-selective responses were observed in one subpopulation, while early nonselective inhibition, followed later by selective excitation was observed in another. This suggests a complex interaction between inputs from other, perhaps auditory areas and local area 32 circuits in processing of sounds including vocalizations. Understanding exactly how this neural dance of dynamics plays out and underpins auditory processing and vocal communication will be the thrust of our future experiments. For now, it seems safe to say that area 32 plays a key role in vocal communication, where integrating context, content, and subtle social cues is essential for coordinating appropriate initiation and response of vocal exchanges. The next time you engage in a conversation, take a moment to appreciate the myriad intricacies of the neural processes involved in this deceptively complex behavior. I always do. 

Cover photo created using ChatGPT under supervision.

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Electrophysiology
Life Sciences > Biological Sciences > Neuroscience > Neurophysiology > Electrophysiology
Social Cognition
Life Sciences > Biological Sciences > Neuroscience > Cognitive Neuroscience > Social Cognition
Neuroscience
Life Sciences > Biological Sciences > Neuroscience
Speech and Audio Processing
Life Sciences > Biological Sciences > Biological Techniques > Computational and Systems Biology > Systems Biology > Signal Processing > Speech and Audio Processing

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