Marmosets: A Neuroscientific Model of Human Social Behavior

Abstract

The common marmoset (Callithrix jacchus) has garnered interest recently as a powerful model for the future of neuroscience research. Much of this excitement has centered on the species' reproductive biology and compatibility with gene editing techniques, which together have provided a path for transgenic marmosets to contribute to the study of disease as well as basic brain mechanisms. In step with technical advances is the need to establish experimental paradigms that optimally tap into the marmosets' behavioral and cognitive capacities. While conditioned task performance of a marmoset can compare unfavorably with rhesus monkey performance on conventional testing paradigms, marmosets' social behavior and cognition are more similar to that of humans. For example, marmosets are among only a handful of primates that, like humans, routinely pair bond and care cooperatively for their young. They are also notably pro-social and exhibit social cognitive abilities, such as imitation, that are rare outside of the Apes. In this Primer, we describe key facets of marmoset natural social behavior and demonstrate that emerging behavioral paradigms are well suited to isolate components of marmoset cognition that are highly relevant to humans. These approaches generally embrace natural behavior, which has been rare in conventional primate testing, and thus allow for a new consideration of neural mechanisms underlying primate social cognition and signaling. We anticipate that through parallel technical and paradigmatic advances, marmosets will become an essential model of human social behavior, including its dysfunction in neuropsychiatric disorders.

Figure 1

Cladogram showing the evolutionary divergence between humans, rodents and each of the main primate taxonomic groups, and estimated time points of divergence. [MYA-Millions of Years Ago].

Figure 2

Scan patterns of a marmoset attending to social stimuli (Mitchell et al., 2014). Note the repeated saccades to the face in each image. In panel B, the first saccade away from the face was in the direction of the gaze.

Figure 3

Evidence of the ‘Face-Patch’ system in the extrastriate cortex of marmosets (Hung et al., 2015). fMRI functional map contrasting faces and objects reveals five discrete areas that significantly more responsive to face stimuli in awake marmosets. A sixth face patch, indicated by a red circle and labeled area MV, was detected with ECoG but not with fMRI due to signal dropout. Color bar below represents the t value scale.

Figure 4

Antiphonal calling conversations in marmosets. (A) Plots spectrograms of two visually occluded marmosets engaged in an antiphonal conversational exchange. The vocalizations of each individual monkey is shown in the spectrogram shown on each row. A 2-pulse Phee call is indicated at the top. (B) Shows an antiphonal conversation between a live marmoset (above) Virtual Marmoset (VM; below). Note that marmosets directly engage VMs similarly to live marmosets. This behavioral paradigm affords the unique opportunity to actively participate in primate social signaling while also maintaining experimental control for explicit tests of social recognition and decision-making.

Figure 5

Vocal-motor activity in marmoset frontal cortex neurons during natural vocal production (Miller et al., 2015). Two representative examples of neurons recorded during natural vocal production are shown. A schematic drawing at top shows the anatomical location of each cell in marmoset frontal cortex. Below plots the response during vocal production (Raster and PSTH). Grey bars on each line of the Raster plot the onset and offset of each 2-pulse phee, while vertical black lines indicate an action potential. The red vertical lines in the PSTH indicate the average onset and offset of each pulse of the phee.