Evolution of the Octavolateral Efferent System

Köppl, Christine

doi:10.1007/978-1-4419-7070-1_8

Cited by 31 publications

(40 citation statements)

References 208 publications

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“…By the early 1990s, a common theme of efferent neurons being associated with the facial motoneurons emerged [Roberts and Meredith, 1992;Köppl, 2011]. In fact, the facial motoneurons have been implied to be among the earliest chordate motoneurons [Dufour et al, 2006], consistent with the finding of efferent terminals on sensory cells in chordates that have certain features in common with hair cells [Burighel et al, 2011].…”

Section: Evolutionary Origin Of Efferent Innervation To Hair Cellssupporting

confidence: 61%

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Sienknecht¹,

Köppl²,

Fritzsch

2014

Brain Behav Evol

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The function of the inner ear critically depends on mechanoelectrically transducing hair cells and their afferent and efferent innervation. The first part of this review presents data on the evolution and development of polarized vertebrate hair cells that generate a sensitive axis for mechanical stimulation, an essential part of the function of hair cells. Beyond the cellular level, a coordinated alignment of polarized hair cells across a sensory epithelium, a phenomenon called planar cell polarity (PCP), is essential for the organ's function. The coordinated alignment of hair cells leads to hair cell orientation patterns that are characteristic of the different sensory epithelia of the vertebrate inner ear. Here, we review the developmental mechanisms that potentially generate molecular and morphological asymmetries necessary for the control of PCP. In the second part, this review concentrates on the evolution, development and function of the enigmatic efferent neurons terminating on hair cells. We present evidence suggestive of efferents being derived from motoneurons and synapsing predominantly onto a unique but ancient cholinergic receptor. A review of functional data shows that the plesiomorphic role of the efferent system likely was to globally shut down and protect the peripheral sensors, be they vestibular, lateral line or auditory hair cells, from desensitization and damage during situations of self-induced sensory overload. The addition of a dedicated auditory papilla in land vertebrates appears to have favored the separation of vestibular and auditory efferents and specializations for more sophisticated and more diverse functions.

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Section: Evolutionary Origin Of Efferent Innervation To Hair Cellssupporting

confidence: 61%

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Sienknecht¹,

Köppl²,

Fritzsch

2014

Brain Behav Evol

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“…A prior study showed that spiking activity in putative AE axons of the eighth nerve increases in most recordings during fictive vocalizations (Weeg et al, 2005), consistent with our finding of depolarizing potentials in central recordings from AE neurons. These hindbrain neurons, like their olivocochlear homologs (Köppl, 2011), are activated by a variety of sensory stimuli (Highstein and Baker, 1985;Tricas and Highstein, 1990;Delano et al, 2007;Köppl, 2011). Hence, their dendritic arbor requires integration of neuronal inputs from multiple sources, including the vocal activity shown in our results.…”

Section: Duration Versus Prr/frequency Transmissionmentioning

confidence: 56%

“…One potential target for a VCD are hindbrain neurons common to all vertebrates that provide efferent input to auditory hair cells in the inner ear (Roberts and Meredith, 1992;Weeg et al, 2005;Köppl, 2011). In midshipman, these auditory efferent (AE) neurons also receive direct input from the vocal CPG (vocal prepacemaker nucleus [VPP], Fig.…”

Section: Introductionmentioning

confidence: 99%

Vocal Corollary Discharge Communicates Call Duration to Vertebrate Auditory System

Chagnaud

Bass

2013

J. Neurosci.

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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.

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“…The first pathway includes TH-ir (DA) neurons in the TPp that project directly to the base of sensory hair cells in the main endorgan of hearing, the saccule, via nerve VIII, while the second, indirect pathway, which also appears to originate in the TPp, is a massive TH-ir input on the dendrites and somata of the OE, which in turn projects to the inner ear and lateral line organs Bleckmann et al, 1991;Highstein and Baker, 1986;Highstein et al, 1992;Koppl, 2011;Tomchik and Lu, 2005;Weeg et al, 2005). To our knowledge this is the first demonstration of catecholaminergic terminals in the sensory epithelium of the inner ear of any non-mammalian vertebrate, and suggests a conserved and important anatomical and functional role for dopamine in normal audition.…”

Section: Th-ir Neurons In the Periventricular Posterior Tuberculum Hamentioning

confidence: 99%

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

Forlano

Kim

Krzyminska

et al. 2014

J of Comparative Neurology

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Although the neuroanatomical distribution of catecholaminergic (CA) neurons has been well documented across all vertebrate classes, few studies have examined CA connectivity to physiologically and anatomically identified neural circuitry that controls behavior. The goal of this study was to characterize CA distribution in the brain and inner ear of the plainfin midshipman fish (Porichthys notatus) with particular emphasis on their relationship with anatomically labeled circuitry that both produces and encodes social acoustic signals in this species. Neurobiotin labeling of the main auditory endorgan, the saccule, combined with tyrosine hydroxylase immunofluorescence (TH-ir) revealed a strong CA innervation of both the peripheral and central auditory system. Diencephalic TH-ir neurons in the periventricular posterior tuberculum, known to be dopaminergic, send ascending projections to the ventral telencephalon and prominent descending projections to vocal-acoustic integration sites, notably the hindbrain octavolateralis efferent nucleus, as well as onto the base of hair cells in the saccule via nerve VIII. Neurobiotin backfills of the vocal nerve in combination with TH-ir revealed CA terminals on all components of the vocal pattern generator which appears to largely originate from local TH-ir neurons but may include diencephalic projections as well. This study provides strong evidence for catecholamines

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Evolution of the Octavolateral Efferent System

Cited by 31 publications

References 208 publications

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Evolution and Development of Hair Cell Polarity and Efferent Function in the Inner Ear

Vocal Corollary Discharge Communicates Call Duration to Vertebrate Auditory System

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

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