Dataset Information

Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus.

ABSTRACT: Auditory streaming enables perception and interpretation of complex acoustic environments that contain competing sound sources. At early stages of central processing, sounds are segregated into separate streams representing attributes that later merge into acoustic objects. Streaming of temporal cues is critical for perceiving vocal communication, such as human speech, but our understanding of circuits that underlie this process is lacking, particularly at subcortical levels. The superior paraolivary nucleus (SPON), a prominent group of inhibitory neurons in the mammalian brainstem, has been implicated in processing temporal information needed for the segmentation of ongoing complex sounds into discrete events. The SPON requires temporally precise and robust excitatory input(s) to convey information about the steep rise in sound amplitude that marks the onset of voiced sound elements. Unfortunately, the sources of excitation to the SPON and the impact of these inputs on the behavior of SPON neurons have yet to be resolved. Using anatomical tract tracing and immunohistochemistry, we identified octopus cells in the contralateral cochlear nucleus (CN) as the primary source of excitatory input to the SPON. Cluster analysis of miniature excitatory events also indicated that the majority of SPON neurons receive one type of excitatory input. Precise octopus cell-driven onset spiking coupled with transient offset spiking make SPON responses well-suited to signal transitions in sound energy contained in vocalizations. Targets of octopus cell projections, including the SPON, are strongly implicated in the processing of temporal sound features, which suggests a common pathway that conveys information critical for perception of complex natural sounds.

SUBMITTER: Felix Ii RA

PROVIDER: S-EPMC5449481 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus.

Felix Ii Richard A RA Gourévitch Boris B Gómez-Álvarez Marcelo M Leijon Sara C M SCM Saldaña Enrique E Magnusson Anna K AK

Frontiers in neural circuits 20170531

Auditory streaming enables perception and interpretation of complex acoustic environments that contain competing sound sources. At early stages of central processing, sounds are segregated into separate streams representing attributes that later merge into acoustic objects. Streaming of temporal cues is critical for perceiving vocal communication, such as human speech, but our understanding of circuits that underlie this process is lacking, particularly at subcortical levels. The superior paraol ...[more]

PMID: 28620283

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Project description:Electrophysiological studies from mice in vitro have suggested that octopus cells of the mammalian ventral cochlear nucleus (VCN) are anatomically and biophysically specialized for detecting the coincident firing of a population of auditory nerve fibers. Recordings from cats in vivo have shown that octopus cells fire rapidly and with exceptional temporal precision as they convey the timing of that coincidence to higher auditory centers. The current study addresses the question whether the biophysical properties of octopus cells that have until now been examined only in mice, are shared by octopus cells in cats. Whole-cell patch-clamp recordings confirm that octopus cells in brain slices from kittens share the anatomical and biophysical features of octopus cells in mice. As in mice, octopus cells in kittens have large cell bodies and thick dendrites that extend in one direction. Voltage changes produced by depolarizing and hyperpolarizing current injection were small and rapid. Input resistances and membrane time constants in octopus cells of 16-day-old kittens were 15.8 +/- 1.5 MOmega (n = 16) and 1.28 +/- 0.3 ms (n = 16), respectively. Octopus cells fired only a single action potential at the onset of a depolarizing current pulse; suprathreshold stimuli were greater than 1.8 nA. A tetrodotoxin (TTX)-sensitive sodium conductance (gNa) was responsible for the generation of the action potentials. Octopus cells displayed outward rectification that lasted for the duration of the depolarizing pulses. Hyperpolarizations produced by the injection of current exhibited a depolarizing sag of the membrane potential toward the resting value. A 4-aminopyridine (4-AP) and alpha-dendrotoxin (alpha-DTX)-sensitive, low-voltage-activated potassium conductance (gKL) and a ZD7288-sensitive, mixed-cation conductance (gh) were partially activated at rest, giving the octopus cells low input resistances and, as a consequence, brief time constants. In 7-day-old kittens, action potentials were taller and broader, input resistances higher, and both inward and outward rectification was weaker than in 16-day-old kittens. Also as in mice, stellate cells of the VCN fired trains of action potentials with constant interspike intervals when they were depolarized (n = 10) and bushy cells of the VCN fired only a single action potential at the onset of depolarizations (n = 6). In conclusion, the similarity of octopus cells in mice and kittens suggests that the anatomical and biophysical specializations that allow octopus cells to detect and convey synchronous firing among auditory nerve fibers are common to all mammals.

Dataset Information

Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus.

Publications

Octopus Cells in the Posteroventral Cochlear Nucleus Provide the Main Excitatory Input to the Superior Paraolivary Nucleus.

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