Auditory cortical regions show resting-state functional connectivity with the default mode-like network in echolocating bats

• Published in: Proceedings of the National Academy of Sciences - PNAS 2024-07, Vol.121 (27), p.e2306029121
• Main Authors: Washington, Stuart D, Shattuck, Kyle, Steckel, Jan, Peremans, Herbert, Jonckers, Elisabeth, Hinz, Rukun, Venneman, Tom, Van den Berg, Monica, Van Ruijssevelt, Lisbeth, Verellen, Thomas, Pritchett, Dominique L, Scholliers, Jan, Liang, Sayuan, C Wang, Paul, Verhoye, Marleen, Esser, Karl-Heinz, Van der Linden, Annemie, Keliris, Georgios A
• Format: Article
• Language: English
• Subjects: Animals; Auditory Cortex - diagnostic imaging; Auditory Cortex - physiology; Basal ganglia; Bats; Biological Sciences; Brain stem; Cerebellum; Chiroptera - physiology; Cognition; Cortex (cingulate); Cortex (parietal); Data acquisition; Default Mode Network - diagnostic imaging; Default Mode Network - physiology; Discoloration; Echolocation; Echolocation - physiology; Female; Functional magnetic resonance imaging; Ganglia; Hearing; Independent component analysis; Magnetic Resonance Imaging; Male; Nerve Net - diagnostic imaging; Nerve Net - physiology; Networks; Phyllostomus discolor; Ripples; Social interactions; Social organization; Social Sciences; Substrates
• ISSN: 0027-8424; 1091-6490; 1091-6490
• DOI: 10.1073/pnas.2306029121

Echolocating bats are among the most social and vocal of all mammals. These animals are ideal subjects for functional MRI (fMRI) studies of auditory social communication given their relatively hypertrophic limbic and auditory neural structures and their reduced ability to hear MRI gradient noise. Yet, no resting-state networks relevant to social cognition (e.g., default mode-like networks or DMLNs) have been identified in bats since there are few, if any, fMRI studies in the chiropteran order. Here, we acquired fMRI data at 7 Tesla from nine lightly anesthetized pale spear-nosed bats ( ). We applied independent components analysis (ICA) to reveal resting-state networks and measured neural activity elicited by noise ripples (on: 10 ms; off: 10 ms) that span this species' ultrasonic hearing range (20 to 130 kHz). Resting-state networks pervaded auditory, parietal, and occipital cortices, along with the hippocampus, cerebellum, basal ganglia, and auditory brainstem. Two midline networks formed an apparent DMLN. Additionally, we found four predominantly auditory/parietal cortical networks, of which two were left-lateralized and two right-lateralized. Regions within four auditory/parietal cortical networks are known to respond to social calls. Along with the auditory brainstem, regions within these four cortical networks responded to ultrasonic noise ripples. Iterative analyses revealed consistent, significant functional connectivity between the 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 highly social and vocal species.