Hair cell and neural contributions to the cochlear summating potential

Abstract

The cochlear summating potential (SP) to a tone is a baseline shift that persists for the duration of the burst. It is often considered the most enigmatic of cochlear potentials because its magnitude and polarity vary across frequency and level and its origins are uncertain. In this study, we used pharmacology to isolate sources of the SP originating from the gerbil cochlea. Animals either had the full complement of outer and inner hair cells (OHCs and IHCs) and an intact auditory nerve or had systemic treatment with furosemide and kanamycin (FK) to remove the outer hair cells. Responses to tone bursts were recorded from the round window before and after the neurotoxin kainic acid (KA) was applied. IHC responses were then isolated from the post-KA responses in FK animals, neural responses were isolated from the subtraction of post-KA from pre-KA responses in NH animals, and OHC responses were isolated by subtraction of post-KA responses in FK animals from post-KA responses in normal hearing (NH) animals. All three sources contributed to the SP; OHCs with a negative polarity and IHCs and the auditory nerve with positive polarity. Thus the recorded SP in NH animals is a sum of contributions from different sources, contributing to the variety of magnitudes and polarities seen across frequency and intensity. When this information was applied to observations of the SP recorded from the round window in human cochlear implant subjects, a strong neural contribution to the SP was confirmed in humans as well as gerbils. NEW & NOTEWORTHY Of the various potentials produced by the cochlea, the summating potential (SP) is typically described as the most enigmatic. Using combinations of ototoxins and neurotoxins, we show contributions to the SP from the auditory nerve and from inner and outer hair cells, which differ in polarity and vary in size across frequency and level. This complexity of sources helps to explain the enigmatic nature of the SP.

The frequency limit of outer hair cell motility measured in vivo

“…Overall our data suggest that OHCs and IHCs have similar properties, namely, considerable rectification (Pappa et al, 2019) and a corner frequency not exceeding a few kilohertz. Thus, just like in high-frequency IHCs, the receptor potential of high-frequency OHCs is expected to mainly follow the envelope of the waveform that stimulates their hair bundles.…”

Auditory Neuropathy Spectrum Disorders: From Diagnosis to Treatment: Literature Review and Case Reports

“…OHCs are the main contributors to the generation of an early evoked response, the cochlear microphonic (CM), a short-latency potential occurring before wave I of the ABRs. It has been shown that CM originates from the mechano-sensitive transduction channels in the stereocilia of both IHCs and OHCs, with a predominance for the OHCs due to their greater number, and is produced by the opening and closing of transduction channels in the hair bundle that follow the movement of the basilar membrane [144,145]. The CM is an electrophysiological response that is polarity dependent.…”

“…The origins of SP are more debated and remain unclear, but it is accepted that SP mainly reflects the activity of IHCs [152]. More recently, the effects of ototoxins and neurotoxins in animal models suggested a possible combined receptor and neural origin of the SP [144].…”

“…Despite preserved hearing in quiet, patient complaints of poor speech understanding in challenging hearing conditions, especially with background noise. basilar membrane [144,145]. The CM is an electrophysiological response that is polarity dependent.…”

Light sheet microscopy of the gerbil cochlea

“…Here, using LSFM of the gerbil cochlea, we demonstrate that the cochlea's three-dimensional frequency structure can be preserved, displayed, and measured. These measures are of great interest to physiologists investigating the cellular origins of the complex waveforms generated by the cochlea in response to acoustic (e.g., Forgues et al, 2014;Pappa et al, 2019) or electrical (e.g., Li, Lu, Zhang, Hansen, & Li, 2020;Wiegner, Wright, & Vollmer, 2016) stimuli, for monitoring changes in intracochlear pressure levels at defined frequency locations (e.g., Kale & Olson, 2015) F I G U R E 1 8 Application of the three-dimensional frequency map for geometry based physiological investigations. Frequency maps from otic capsule intact specimens retain relationships with external structures, as viewed from the apex (a) or laterally (b).…”