Schaeffer DJ, Gilbert KM, Bellyou M, Silva AC, Everling S (2022). Frontoparietal network connectivity as a product of convergent evolution in rodents and primates: functional con-nectivity topologies in grey squirrels, rats, and marmosets. Communications Biology 5 (1): 986
Robust frontoparietal connectivity is a defining feature of primate cortical organization. Whether mammals outside the primate order, such as rodents, possess similar frontoparietal functional connectivity organization is a controversial topic. Previous work has primarily focused on comparing mice and rats to primates. However, as these rodents are nocturnal and terrestrial, they rely much less on visual input than primates. Here, we investigated the functional cortical organization of grey squirrels which are diurnal and arboreal, thereby better resembling primate ecology. We used ultra-high field resting-state fMRI data to compute and compare the functional connectivity patterns of frontal regions in grey squirrels (Sciurus carolinensis), rats (Rattus norvegicus), and marmosets (Callithrix jacchus). We utilized a fingerprinting analysis to compare interareal patterns of functional connectivity from seeds across frontal cortex in all three species. The results show that grey squirrels, but not rats, possess a frontoparietal connectivity organization that resembles the connectivity pattern of marmoset lateral prefrontal cortical areas. Since grey squirrels and marmosets have acquired an arboreal way of life but show no common arboreal ancestor, the expansion of the visual system and the formation of a frontoparietal connectivity architecture might reflect convergent evolution driven by similar ecological niches in primates and tree squirrels.
The correct identification of facial expressions is critical for understanding the intention of others during social communication in the daily life of all primates. Here we used ultra-high field fMRI at 9.4T to investigate the neural network activated by facial expressions in awake New World common marmosets from both male and female sex, and to determine the effect of facial motions on this network. We further explored how the face-patch network is involved in the processing of facial expressions. Our results show that dynamic and static facial expressions activate face-patches in temporal and frontal areas (O, PV, PD, MD, AD and PL) as well as the amygdala, with stronger responses for negative faces, also associated with an increase of the monkey's respiration rates. Processing of dynamic facial expressions involves an extended network recruiting additional regions not known to be part of the face-processing network, suggesting that face motions may facilitate the recognition of facial expressions.We report for the first time in New World marmosets that the perception and identification of changeable facial expressions, vital for social communication, recruit face-selective brain patches also involved in face detection processing, and are associated with an increase of arousal.
Background: The small common marmoset (Callithrix jacchus) is an ideal nonhuman primate for awake fMRI in ultra-high field small animal MRI scanners. However, it can often be challenging in task-based fMRI experiments to provide a robust stimulus within the MRI environment while using hardware (an RF coil and restraint system) that is compatible with awake imaging.
New method: Here we present an RF coil and restraint system that permits unimpeded access to an awake marmoset's head subsequent to immobilization, thereby permitting the setup of peripheral devices and stimuli proximal to the head.
Results: As an example application, an fMRI experiment probing whole-brain activation in response to marmoset vocalizations was conducted-this paradigm showed significant bilateral activation in the inferior colliculus, medial lateral geniculate nucleus, and auditory cortex.
Comparison with existing method(s): The coil performance was evaluated and compared to a previously published restraint system with integrated RF coil. The image and temporal SNR were improved by up to 58 % and 27 %, respectively, in the peripheral cortex and by 30 % and 3 % in the centre of the brain. The restraint-system topology limited head motion to less than 100 µm of translation and 0.30° of rotation when measured over a 15-minute acquisition.
Conclusions: The proposed hardware solution provides a versatile approach to awake-marmoset imaging and, as demonstrated, can facilitate task-based fMRI.