Vocal‐motor and auditory connectivity of the midbrain periaqueductal gray in a teleost fish

Abstract

The midbrain periaqueductal gray (PAG) plays a central role in the descending control of vocalization across vertebrates. The PAG has also been implicated in auditory-vocal integration, though its precise role in such integration remains largely unexplored. Courtship and territorial interactions in plainfin midshipman fish depend on vocal communication, and the PAG is a central component of the midshipman vocal-motor system. We made focal neurobiotin injections into the midshipman PAG to both map its auditory-vocal circuitry and enable evolutionary comparisons with tetrapod vertebrates. These injections revealed an extensive bidirectional pattern of connectivity between the PAG and known sites in both the descending vocal-motor and ascending auditory systems, including portions of the telencephalon, dorsal thalamus, hypothalamus, posterior tuberculum, midbrain and hindbrain. Injections in the medial PAG produced dense label within hindbrain auditory nuclei, while those confined to the lateral PAG preferentially labeled hypothalamic and midbrain auditory areas. Thus, the teleost PAG may have functional subdivisions playing different roles in vocal-auditory integration. Together, the results confirm several pathways previously identified by injections into known auditory or vocal areas and provide strong support for the hypothesis that the teleost PAG is centrally involved in auditory-vocal integration.

Melatonin action in a midbrain vocal-acoustic network

“…In midshipman fish, the midbrain PAG is a crucial node in vocalization initiation and is highly interconnected with auditory centers, consistent with its role in sensorimotor integration and vocal initiation in birds and mammals (Jürgens, 2009;Holstege, 1989;Kingsbury et al, 2011;Kittelberger and Bass, 2013). A recent study revealed that the midshipman lateral PAG is more extensively connected than the medial PAG to auditory-recipient nuclei including the TSd (Kittelberger and Bass, 2013), consistent with our finding that TSd stimulation can elicit longer calls (supplementary material Fig.…”

“…Within the midshipman vocal network, the midbrain periaqueductal gray (PAG) and surrounding midbrain tegmentum play a crucial role in vocalization initiation, consistent with other vertebrates (Kittelberger and Bass, 2013). We report that, compared with medial stimulation sites, lateral midbrain sites produce longer duration calls comparable to natural advertisement/mate calls that are more sensitive to the stimulatory effects of melatonin than brief calls evoked from medial sites.…”

“…In addition to eliciting vocal output from medial sites in the medial PAG and nearby tegmentum (Kittelberger and Bass, 2013), we also stimulated sites in the lateral midbrain that could reliably elicit up to a magnitude longer duration output. We first provide evidence of photoregime effects and melatonin modulation in medial and lateral midbrain regions followed by detailed comparisons of their excitability.…”

“…We showed that activation of medial and lateral midbrain regions led to short-or long-duration calls, respectively. The vocally active sites identified here are inclusive of those anatomically mapped in prior studies of midshipman fish (Goodson and Bass, 2002;Kittelberger et al, 2006;Kittelberger and Bass, 2013). Whether medial and lateral sites represent two parallel subdivisions of the descending vocal system or the lateral midbrain feeds into the medial to activate the hindbrain vocal central pattern generator (CPG) is beyond the scope of this study and requires further investigation of midbrain microcircuitry.…”

Vocal Corollary Discharge Communicates Call Duration to Vertebrate Auditory System

“…2B). Consistent with direct input from the vocally active midbrain periaqueductal gray to AE neurons (Kittelberger and Bass, 2013), electrical stimulation in the periaqueductal gray region led to synaptic responses in AE neurons (Fig. 3B).…”