Innovations in motoneuron synchrony drive rapid temporal modulations in vertebrate acoustic signaling

Abstract

Rapid temporal modulation of acoustic signals among several vertebrate lineages has recently been shown to depend on the actions of superfast muscles. We hypothesized that such fast events, known to require synchronous activation of muscle fibers, would rely on motoneuronal properties adapted to generating a highly synchronous output to sonic muscles. Using intracellular in vivo recordings, we identified a suite of premotor network inputs and intrinsic motoneuronal properties synchronizing the oscillatory-like, simultaneous activation of superfast muscles at high gamma frequencies in fish. Motoneurons lacked spontaneous activity, firing synchronously only at the frequency of premotor excitatory input. Population-level motoneuronal output generated a spike-like, vocal nerve volley that directly determines muscle contraction rate and, in turn, natural call frequency. In the absence of vocal output, motoneurons showed low excitability and a weak afterhyperpolarization, leading to rapid accommodation in firing rate. By contrast, vocal activity was accompanied by a prominent afterhyperpolarization, indicating a dependency on network activity. Local injection of a GABA(A) receptor antagonist demonstrated the necessity of electrophysiologically and immunohistochemically confirmed inhibitory GABAergic input for motoneuronal synchrony and vocalization. Numerous transneuronally labeled motoneurons following single-cell neurobiotin injection together with electrophysiological collision experiments confirmed gap junctional coupling, known to contribute to synchronous activity in other neural networks. Motoneuronal synchrony at the premotor input frequency was maintained during differential recruitment of variably sized motoneurons. Differential motoneuron recruitment led, however, to amplitude modulation (AM) of vocal output and, hence, natural call AM. In summary, motoneuronal intrinsic properties, in particular low excitability, predisposed vocal motoneurons to the synchronizing influences of premotor inputs to translate a temporal input code into a coincident and extremely synchronous, but variable-amplitude, output code. We propose an analogous suite of neuronal properties as a key innovation underlying similarly rapid acoustic events observed among amphibians, reptiles, birds, and mammals.

Vocal Corollary Discharge Communicates Call Duration to Vertebrate Auditory System

“…1B) that matches the activity of single motoneurons ( Fig. 1C) (Bass and Baker, 1990;Chagnaud et al, 2012). The patterning of motoneuron activity, and hence fictive and natural grunts, is determined by separate hindbrain populations coding for duration, PRR/frequency, and amplitude within a vocal central pattern generator (CPG) that includes the vocal motor nucleus (Fig.…”

“…Fish were fed on a weekly diet of goldfish. All procedures followed previously described methods (Chagnaud et al, 2011) and were approved by the Cornell University Institutional Animal Care and Use Committee.…”

“…In midshipman, these auditory efferent (AE) neurons also receive direct input from the vocal CPG (vocal prepacemaker nucleus [VPP], Fig. 1B) (Chagnaud et al, 2011). Here, intracellular recordings show that AE neurons generate a VCD specifically adapted for the coding of call duration, a major acoustic attribute for midshipman fish and sonic vertebrates in general (Bass and McKibben, 2003;Bradbury and Vehrencamp, 2011).…”

“…1A, top left) (Bass and McKibben, 2003). Vocalization results from the simultaneous contraction of paired swim bladder muscles in response to synchronous input from vocal nerves homologous to hypoglossal roots that innervate avian syringeal muscles (Bass et al, 2008). Vocal nerve activity directly determines both the rate at which individual calls, such as grunts, are produced (Fig.…”

“…The patterning of motoneuron activity, and hence fictive and natural grunts, is determined by separate hindbrain populations coding for duration, PRR/frequency, and amplitude within a vocal central pattern generator (CPG) that includes the vocal motor nucleus (Fig. 1B) (Chagnaud et al, 2011(Chagnaud et al, , 2012.…”