Midbrain Periaqueductal Gray and Vocal Patterning in a Teleost Fish

Abstract

Midbrain structures, including the periaqueductal gray (PAG), are essential nodes in vertebrate motor circuits controlling a broad range of behaviors, from locomotion to complex social behaviors such as vocalization. Few single-unit recording studies, so far all in mammals, have investigated the PAG's role in the temporal patterning of these behaviors. Midshipman fish use vocalization to signal social intent in territorial and courtship interactions. Evidence has implicated a region of their midbrain, located in a similar position as the mammalian PAG, in call production. Here, extracellular single-unit recordings of PAG neuronal activity were made during forebrain-evoked fictive vocalizations that mimic natural call types and reflect the rhythmic output of a known hindbrain-spinal pattern generator. The activity patterns of vocally active PAG neurons were mostly correlated with features related to fictive call initiation. However, spike trains in a subset of neurons predicted the duration of vocal output. Duration is the primary feature distinguishing call types used in different social contexts and these cells may play a role in directly establishing this temporal dimension of vocalization. Reversible, lidocaine inactivation experiments demonstrated the necessity of the midshipman PAG for fictive vocalization, whereas tract-tracing studies revealed the PAG's connectivity to vocal motor centers in the fore- and hindbrain comparable to that in mammals. Together, these data support the hypotheses that the midbrain PAG of teleosts plays an essential role in vocalization and is convergent in both its functional and structural organization to the PAG of mammals.

Plasticity in Brain Sexuality Is Revealed by the Rapid Actions of Steroid Hormones

“…The midbrain site used here and previously (Bass and Baker, 1990;Remage-Healey and Bass, 2004) projects directly to the VPG (Fig. 1 A) (Goodson and Bass, 2002;Kittelberger et al, 2006). Fictive calls were recorded with an extracellular electrode (Teflon-coated silver wire with exposed ball tip 50 -100 m in diameter) placed on a ventral occipital nerve root that innervates the ipsilateral sonic muscle (Fig.…”

Central pattern generators for social vocalization: Androgen-dependent neurophysiological mechanisms

“…Functional similarities between the vocal control systems of batrachoidids and tetrapods are highlighted by the most recent single neuron recording study showing the essential role played by the PAG in call initiation (Kittelberger et al, 2006). Perhaps somewhat remarkably, the neurophysiological properties of PAG neurons closely resemble those of mammals, including primates (see Kittelberger et al, 2006 and discussion therein).…”

“…Early studies provided concurrent recordings of vocalizations and electromyograms and/or action potentials from the swim bladder muscles of Opsanus tau and the plainfin midshipman Porichthys notatus to show that the simultaneous contraction of both muscles is matched 1:1 with each sound pulse (Skoglund, 1961;Cohen and Winn, 1967). Neurophysiological analyses of the CNS of batrachoidids have roots in intracellular recording studies of electrotonic coupling in the vocal motor system of the oyster toadfish O. tau (Pappas and Bennett, 1966), and brain stimulation studies of the Gulf toadfish Opsanus beta that mapped vocally active sites throughout the CNS (Demski and Gerald, 1972;see Fine andPerini, 1994 andKittelberger et al, 2006 for overviews of subsequent studies).…”

“…The midbrain vocal-auditory center includes the periaqueductal gray (PAG) that links forebrain vocal sites (fVAC, Fig. 1A) to the vocal CPG at hindbrain-spinal levels (Goodson and Bass, 2002;Kittelberger et al, 2006). Functional similarities between the vocal control systems of batrachoidids and tetrapods are highlighted by the most recent single neuron recording study showing the essential role played by the PAG in call initiation (Kittelberger et al, 2006).…”

Sensory feedback control of mammalian vocalizations

“…The relative significance of each individual feedback mechanism may vary among mammals depending upon the nature and sophistication of each species' unique vocal repertoire, but a wealth of evidence supports the conclusion that all mammals, including humans, share a basically similar functional neuroanatomical organization of the vocal sensory-motor integration pathways [60]. To a large extent these similarities extend to other vertebrates, notably including songbirds [58], chorusing frogs [7], and even fish [35,67]. Ultimately the neural substrate for human speech will perhaps be distinguished by its more elaborate and sophisticated cortical circuitry [88], but surprisingly, many of the normal ways in which human speech responds to sensory feedback, such as in the case of the Lombard effect [76] or the response to pitch-shifted feedback [9,23], have been documented in a variety of other animals [54,113,116,135].…”