Chiropteran neuroimaging : structural and functional magnetic resonance imaging of the pale spear-nosed bat

Echolocating bats live huddled together in colonies comprising hundreds of individuals and use complex sounds to communicate and to navigate. These highly social and vocal species make ideal subjects for functional magnetic resonance imaging (fMRI) studies of auditory social communication given their relatively hypertrophic limbic and auditory neural structures and their reduced ability to hear MRI gradient noise. Establishing the existence of neural networks related to social cognition (e.g., default mode-like networks or DMLNs) in order Chiroptera could pave the way towards a new frontier in the study of mammalian socialization and communication. We measured blood oxygenation level dependent (BOLD) signal at 7T from nine lightly anesthetized pale spear-nosed bats (Phyllostomus discolor). Specifically, we performed independent components analysis (ICA) and revealed 15 resting-state networks. We also measured neural activity elicited by noise ripples (on: 10 ms; off: 10 ms) that span the ultrasonic hearing range (20-130 kHz) of this species. Resting-state networks intersected parietal, occipital, and auditory cortices, along with auditory brainstem, basal ganglia, cerebellum, and hippocampus. We determined that two out of a possible four midline networks were the best candidates for DMLN. We also found two predominantly left and two predominantly right auditory/parietal cortical networks. Regions within all four auditory/parietal cortical networks have been demonstrated to respond to social calls. As expected by the emergence of side-band inhibition in the inferior colliculus, ultrasonic noise ripples significantly activated the auditory brainstem (NOISE>SILENCE- cluster-level: p=5.27 x 10-5, FWE correction, kE=7613) yet deactivated the auditory/parietal cortex (SILENCE>NOISE- cluster-level: p=2.08 x 10-9, FWE correction, kE=17452). Iterative (“jack knife”) analyses revealed consistent, significant functional connections between left, but not right, auditory/parietal cortical networks and DMLN nodes, especially the anterior-most cingulate cortex. Thus, a resting-state network implicated in social cognition displays more distributed functional connectivity across left, relative to right, hemispheric cortical substrates of audition and communication in this echolocating bat species. The application of advanced histological methods to 12 ex-vivo Phyllostomus discolor brain samples that have also undergone structural imaging (i.e., T2-weighted 3D rapid spin echo and spin-echo diffusion weighted) increase the likelihood of generating detailed, 3D population-based atlases as a computerized anatomical reference for these and future chiropteran functional neuroimaging results.