Vocal Corollary Discharge Communicates Call Duration to Vertebrate Auditory System

Abstract

Corollary discharge is essential to an animal's ability to filter self-generated from external stimuli. This includes acoustic communication, although direct demonstration of a corollary discharge that both conveys a vocal motor signal and informs the auditory system about the physical attributes of a self-generated vocalization has remained elusive for vertebrates. Here, we show the underlying synaptic activity of a neuronal vocal corollary discharge pathway in the hindbrain of a highly vocal species of fish. Neurons carrying the vocal corollary discharge are specifically adapted for the transmission of duration information, a predominant acoustic cue. The results reveal that vertebrates, like some insects, have a robust corollary discharge conveying call duration. Along with evidence for the influence of vocal duration on auditory encoding in mammals, these new findings suggest that linking vocal motor and corollary discharge pathways with pattern generating, call duration neurons is a shared network character across the animal kingdom.

Vocal Behavior and Vocal Central Pattern Generator Organization Diverge among Toadfishes

“…In midshipman, single neuron fills show that duration-coding VPP neurons are the principal source of input to the efferent nucleus [Chagnaud et al, 2011]. This finding is consistent with neurophysiological evidence for the robust transfer of duration information by OEN neurons to the auditory (saccule) hair cell epithelium during vocalization, which is hypothesized to decrease auditory reafference [Weeg et al, 2005;Chagnaud and Bass, 2013].…”

“…More extensive single cell anatomy studies of VPN and VPP coupled to intracellular records of target neurons (DOri and OEN) in toadfishes are needed to more rigorously test a predominant role for VPN in vocal coupling to the inner ear and lateral line. Recent intracellular recording studies in midshipman have shown that the VPP is the source of a vocal corollary discharge that informs the auditory system about call duration [Chagnaud and Bass, 2013]. The results presented here for the Gulf toadfish suggest that duration and/or PRR information, both of which are contained within the VPN output, is/are being transferred to the inner ear and lateral line organs.…”

“…The results presented here for the Gulf toadfish suggest that duration and/or PRR information, both of which are contained within the VPN output, is/are being transferred to the inner ear and lateral line organs. As proposed in midshipman fishes [Chagnaud and Bass, 2013], the high fundamental frequency/PRR (>150 Hz) code of the Gulf toadfish will ultimately be turned into a duration code by OEN neurons via summation of excitatory postsynaptic potentials, due to the integrative membrane properties of OEN neurons and the high frequency of VPN activity.…”

“…Comparisons between the current study of Gulf toadfishes and prior ones of plainfin midshipman fishes lead us to propose that: (1) the more expansive dendritic arbor of motoneurons that extensively overlaps an expansive frequency-coding VPN column in the Gulf toadfish contributes to stronger coupling throughout the VMN-VPN circuit which, in turn, is essential for generating stable calls exhibiting prominent FM and AM segments in the Gulf toadfish, (2) robust gap-junction coupling between duration-coding VPP neurons and the VPN-VMN circuit in plainfin midshipman fishes contributes to their ability to generate advertisement calls lasting for minutes to at least 1 h, and (3) vocal coupling to the inner ear and lateral line systems originates mainly from frequency-coding VPN neurons in the Gulf toadfish and duration-coding VPP neurons in the plainfin midshipman. In both species, however, the integrative properties of OEN neurons assure a vocal corollary discharge encoding call duration [Chagnaud and Bass, 2013], one of the most salient cues in auditory perception in vertebrates, including fishes. Importantly, we emphasize that these and related hypotheses are testable using more quantitative neurophysiological methods as we have done in studies of midshipman fishes [Chagnaud et al, 2011Chagnaud and Bass, 2013].…”

Catecholaminergic connectivity to the inner ear, central auditory, and vocal motor circuitry in the plainfin midshipman fish porichthys notatus

“…A hindbrain octavolateral efferent nucleus (OE) receives input from the vocal motor system and projects to the inner ear endorgans and lateral line system Bass et al, 1994;Chagnaud et al, 2011;Chagnaud and Bass, 2013;Weeg et al, 2005). Additionally, the auditory system in midshipman is interconnected to vocal nuclei in the forebrain, midbrain and hindbrain Kittelberger et al, 2006) The goal of this study was to characterize CA distribution in the midshipman brain with particular emphasis on its relationship to identified circuitry that both produces and encodes social acoustic signals.…”