Echolocation reverses information flow in a cortical vocalization network

Abstract

The mammalian frontal and auditory cortices are fundamental structures supporting vocal production, yet the dynamics of information exchange between these regions during vocalization are unknown. Here, we tackle this issue by means of electrophysiological recordings in the fronto-auditory network of freely-vocalizing Carollia perspicillata bats. We find that oscillations in frontal and auditory cortices provide correlates of vocal production with complementary patterns across structures. Causality analyses of oscillatory activity revealed directed information exchange in the network, predominantly of top-down nature (frontal to auditory). Such directed connectivity was dynamic, as it depended on the type of vocalization produced, and on the timing relative to vocal onset. Remarkably, we observed the emergence of bottom-up information transfer only when bats produced calls with evident post-vocal consequences (echolocation pulses). Our results link vocal production to dynamic information transfer between sensory (auditory) and association areas in a highly vocal mammalian animal model.

Neural Processing of Naturalistic Echolocation Signals in Bats

“…What might be even more important than the awake state might be the vocalizing state. Despite of recent technological advances, neural recordings from actively echolocating bats have rarely been conducted ( Sinha and Moss, 2007 ; Kothari et al, 2018 ; Weineck et al, 2020 ; García-Rosales et al, 2022 ). However, it is indisputable that attentional effects occurring during active vocalization may completely alter neural processing of echolocation signals.…”

“…The same study showed that frontal areas, which are likely involved in vocalization initiation, couple their activity with sensory-motor structures such as the striatum after echolocation ( Weineck et al, 2020 ). In addition, information flows between frontal and auditory cortices reverses directionality after bats echolocate ( García-Rosales et al, 2022 ) indicating that the results could be completely different in vocalizing compared to non-vocalizing bats.…”

“…Neural recordings from the auditory cortex and the inferior colliculus, brain regions of great interest when performing experiments in non-vocalizing bats are rare from vocalizing bats ( Kawasaki et al, 1988 ; García-Rosales et al, 2022 ). Neural recordings in vocalizing bats that are stimulated with a replay of previously emitted echolocation signals are necessary to understand how vocalization and attentional processes affect neural coding.…”