Functional neuroanatomy of auditory pathways in the sound-producing fishPollimyrus

Kozloski, James; Crawford, J. Douglas

doi:10.1002/(sici)1096-9861(19981116)401:2<227::aid-cne6>3.0.co;2-r

Cited by 38 publications

(4 citation statements)

References 92 publications

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“…3A, B) [Edds-Walton, 1998b]. Among electroreceptive fishes, both ipsilateral and contralateral otolith organ inputs project directly to the descending octaval nucleus [Bell, 1981; Nieuwenhuys and Pouwels, 1983; Kozlowski and Crawford, 1998]. Given that the earliest fishes are likely to have been electroreceptive [Northcutt, 1980], the binaural nature of the auditory region of the descending octaval nucleus may have been established early in the evolution of fishes.…”

Section: Directional Hearing In Osteichthyesmentioning

confidence: 99%

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Walton

Christensen‐Dalsgaard

Carr

2017

Brain Behav Evol

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The earliest vertebrate ears likely subserved a gravistatic function for orientation in the aquatic environment. However, in addition to detecting acceleration created by the animal's own movements, the otolithic end organs that detect linear acceleration would have responded to particle movement created by external sources. The potential to identify and localize these external sources may have been a major selection force in the evolution of the early vertebrate ear and in the processing of sound in the central nervous system. The intrinsic physiological polarization of sensory hair cells on the otolith organs confers sensitivity to the direction of stimulation, including the direction of particle motion at auditory frequencies. In extant fishes, afferents from otolithic end organs encode the axis of particle motion, which is conveyed to the dorsal regions of first-order octaval nuclei. This directional information is further enhanced by bilateral computations in the medulla and the auditory midbrain. We propose that similar direction-sensitive neurons were present in the early aquatic tetrapods and that selection for sound localization in air acted upon preexisting brain stem circuits like those in fishes. With movement onto land, the early tetrapods may have retained some sensitivity to particle motion, transduced by bone conduction, and later acquired new auditory papillae and tympanic hearing. Tympanic hearing arose in parallel within each of the major tetrapod lineages and would have led to increased sensitivity to a broader frequency range and to modification of the preexisting circuitry for sound source localization.

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Section: Directional Hearing In Osteichthyesmentioning

confidence: 99%

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Walton

Christensen‐Dalsgaard

Carr

2017

Brain Behav Evol

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“…A study on the mormyrid electromotor system confirmed reciprocal connections of the dorsal posterior thalamic nucleus and the ventroposterior toral nucleus with the optic tectum (TeO) ( Carlson, 2002 ). Another study on the mormyrid auditory system showed a projection of the mediodorsal toral nucleus to the TeO ( Kozloski and Crawford, 1998 ). However, the earlier tectal HRP study ( Wullimann and Northcutt, 1990 ) did not investigate topography between torus semicircularis (in particular the lateral toral nucleus) and the TeO, which is the main focus of the present study.…”

Section: Discussionmentioning

confidence: 99%

The Mormyrid Optic Tectum Is a Topographic Interface for Active Electrolocation and Visual Sensing

2018

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The African weakly electric fish Gnathonemus petersii is capable of cross-modal object recognition using its electric sense or vision. Thus, object features stored in the brain are accessible by multiple senses, either through connections between unisensory brain regions or because of multimodal representations in multisensory areas. Primary electrosensory information is processed in the medullary electrosensory lateral line lobe, which projects topographically to the lateral nucleus of the torus semicircularis (NL). Visual information reaches the optic tectum (TeO), which projects to various other brain regions. We investigated the neuroanatomical connections of these two major midbrain visual and electrosensory brain areas, focusing on the topographical relationship of interconnections between the two structures. Thus, the neural tracer DiI was injected systematically into different tectal quadrants, as well as into the NL. Tectal tracer injections revealed topographically organized retrograde and anterograde label in the NL. Rostral and caudal tectal regions were interconnected with rostral and caudal areas of the NL, respectively. However, dorsal and ventral tectal regions were represented in a roughly inverted fashion in NL, as dorsal tectal injections labeled ventral areas in NL and vice versa. In addition, tracer injections into TeO or NL revealed extensive inputs to both structures from ipsilateral (NL also contralateral) efferent basal cells in the valvula cerebelli; the NL furthermore projected back to the valvula. Additional tectal and NL connections were largely confirmatory to earlier studies. For example, the TeO received ipsilateral inputs from the central zone of the dorsal telencephalon, torus longitudinalis, nucleus isthmi, various tegmental, thalamic and pretectal nuclei, as well as other nuclei of the torus semicircularis. Also, the TeO projected to the dorsal preglomerular and dorsal posterior thalamic nuclei as well as to nuclei in the torus semicircularis and nucleus isthmi. Beyond the clear topographical relationship of NL and TeO interconnections established here, the known neurosensory upstream circuitry was used to suggest a model of how a defined spot in the peripheral sensory world comes to be represented in a common associated neural locus both in the NL and the TeO, thereby providing the neural substrate for cross-modal object recognition.

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“…Thus, pathways indicated by the black lines are potentially either excitatory or inhibitory, or may contain both excitatory and inhibitory projections. We created these drawings based on the following literatures: (A) fish, 3,6–11 (B) anuran, 3,12–22 (C) reptile/bird, 23–37 and (D) mammals. 38–65 To emphasize the similarity in the basic organization of the auditory system, we used the terms CN, SO, NLL, and IC for first-, second-, third-order nuclei, and midbrain nucleus.…”

Section: An Overview Of the Inhibitory Neural Circuits In The Auditormentioning

confidence: 99%

“…The IC also receives afferent inputs from the secondary octaval nucleus, SO, and the perilemniscal nucleus. 6,7…”

Section: An Overview Of the Inhibitory Neural Circuits In The Auditormentioning

confidence: 99%

Inhibitory Neural Circuits in the Mammalian Auditory Midbrain

Ono

2018

J Exp Neurosci

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The auditory midbrain is the critical integration center in the auditory pathway of vertebrates. Synaptic inhibition plays a key role during information processing in the auditory midbrain, and these inhibitory neural circuits are seen in all vertebrates and are likely essential for hearing. Here, we review the structure and function of the inhibitory neural circuits of the auditory midbrain. First, we provide an overview on how these inhibitory circuits are organized within different clades of vertebrates. Next, we focus on recent findings in the mammalian auditory midbrain, the most studied of the vertebrates, and discuss how the mammalian auditory midbrain is functionally coordinated.

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Functional neuroanatomy of auditory pathways in the sound-producing fishPollimyrus

Cited by 38 publications

References 92 publications

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

Evolution of Sound Source Localization Circuits in the Nonmammalian Vertebrate Brainstem

The Mormyrid Optic Tectum Is a Topographic Interface for Active Electrolocation and Visual Sensing

Inhibitory Neural Circuits in the Mammalian Auditory Midbrain

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