Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2014 Mar;111(5):930-8.
doi: 10.1152/jn.00648.2013. Epub 2013 Dec 11.

Neuronal interaural level difference response shifts are level-dependent in the rat auditory cortex

Michael Kyweriga  1 , Whitney Stewart, Michael Wehr
Affiliations

Neuronal interaural level difference response shifts are level-dependent in the rat auditory cortex

Michael Kyweriga et al. J Neurophysiol. 2014 Mar.

Abstract

How does the brain accomplish sound localization with invariance to total sound level? Sensitivity to interaural level differences (ILDs) is first computed at the lateral superior olive (LSO) and is observed at multiple levels of the auditory pathway, including the central nucleus of inferior colliculus (ICC) and auditory cortex. In LSO, this ILD sensitivity is level-dependent, such that ILD response functions shift toward the ipsilateral (excitatory) ear with increasing sound level. Thus early in the processing pathway changes in firing rate could indicate changes in sound location, sound level, or both. In ICC, while ILD responses can shift toward either ear in individual neurons, there is no net ILD response shift at the population level. In behavioral studies of human sound localization acuity, ILD sensitivity is invariant to increasing sound levels. Level-invariant sound localization would suggest transformation in level sensitivity between LSO and perception of sound sources. Whether this transformation is completed at the level of the ICC or continued at higher levels remains unclear. It also remains unknown whether perceptual sound localization is level-invariant in rats, as it is in humans. We asked whether ILD sensitivity is level-invariant in rat auditory cortex. We performed single-unit and whole cell recordings in rat auditory cortex under ketamine anesthesia and measured responses to white noise bursts presented through sealed earphones at a range of ILDs. Surprisingly, we found that with increasing sound levels ILD responses shifted toward the ipsilateral ear (which is typically inhibitory), regardless of whether cells preferred ipsilateral, contralateral, or binaural stimuli. Voltage-clamp recordings suggest that synaptic inhibition does not contribute substantially to this transformation in level sensitivity. We conclude that the level invariance of ILD sensitivity seen in behavioral studies is not present in rat auditory cortex.

Keywords: auditory cortex; interaural level difference; level dependence; sound localization.

PubMed Disclaimer

Figures

Fig. 1.
Fig. 1.
Spiking interaural level difference (ILD) responses in the rat auditory cortex shift toward the ipsilateral ear (negative shifts) with increasing ipsilateral sound level. A–F: 2 representative examples showing negative ILD response shifts in both contralateral-preferring (A–C; cell 120810-MK-3-2) and binaural-preferring (D–F; cell 091410-WS-2-1) cells. A and D: spiking responses to the binaural stimulus array. Each histogram shows the firing rate in 20-ms bins (accumulated from 10 trials). White noise bursts (25-ms duration) are indicated in gray. B and E: trial-averaged normalized firing rate heat maps of the same data shown in A and D. Dark red indicates maximum firing rate, and dark blue indicates minimum firing rate. Each binaural stimulus can be represented either as an ILD-average binaural level (ABL) combination (x- and y-axes) or as a contralateral and ipsilateral sound level (diagonal axes). For example, the green response at ILD 20, ABL 20 corresponds to Contra 30, Ipsi 10. C and F: firing rate ILD response curves. Ipsilateral level is held constant for each curve (see inset for color code) as a function of ILD. In other words, each line is a diagonal slice through B, parallel to the Contra axis. C: contralateral-preferring cell with a mean ILD response shift of −0.48 dB/dB (SD = 0.44; see methods for detailed description). Circles denote half-maximal ILD values. Negative ILDs correspond to greater ipsilateral level (Ips > Con); positive ILDs correspond to greater contralateral level (Ips < Con). F: binaural-preferring cell with a mean ILD response shift of −0.76 dB/dB (SD = 0.33). Circles denote the average of left and right half-maximal ILD values; thus the circles are found near the maxima. G: population histograms showing that the majority of cells (89.2%) have negative response shifts (top left, 66/74 cells), regardless of binaural preference categorization (Con, contralateral preferring; Bin, binaural preferring; Ips, ipsilateral preferring).
Fig. 2.
Fig. 2.
Membrane potential (Vm) ILD responses in the rat auditory cortex shift toward the ipsilateral ear with increasing ipsilateral sound level. A–F: 2 representative examples showing negative ILD response shifts in both contralateral-preferring (A–C; cell 010511-MK-3-8) and binaural-preferring (D–F; cell 080910-MK-2-2) nonspiking cells. A and D: membrane potential responses to the binaural stimulus array. Each subplot shows the membrane potential (A: mean of 20 trials; D: mean of 10 trials). White noise bursts (25 ms duration) are indicated in gray. Resting membrane potential (Vrest) is indicated by horizontal thin gray line (A: Vrest = −78.8 mV; D: Vrest = −60.2 mV). Red regions are significantly above baseline and were included in the integrated membrane potential responses in B and C. B and E: normalized integrated membrane potential heat maps of the same data shown in A and D. Dark red indicates maximum depolarization, and dark blue indicates minimum depolarization. C and F: integrated membrane potential ILD response curves. Ipsilateral level held constant for each curve as a function of ILD. C: contralateral-preferring cell with a mean ILD response shift of −0.79 dB/dB (SD = 0.68). F: binaural-preferring cell with a mean ILD response shift of −0.63 dB/dB (SD = 0.33). G: population histograms showing that the majority of cells (95.9%) have negative membrane potential response shifts (top left, 118/123 cells), regardless of binaural preference categorization.
Fig. 3.
Fig. 3.
Synaptic conductance ILD responses in the rat auditory cortex shift toward the ipsilateral ear with increasing ipsilateral sound level. A: representative example showing negative ILD response shifts to both excitatory (GE, green) and inhibitory (GI, red) conductance responses to the binaural stimulus array (cell 072810-MK-3-1). White noise bursts (25-ms duration) are indicated in gray. B and C: integrated synaptic conductance ILD curves (B: excitatory; C: inhibitory). Ipsilateral level held constant for each curve as a function of ILD. This cell was contralateral preferring and had a mean ILD response shift of −0.67 dB/dB for excitation (B; SD = 0.61) and −0.98 dB/dB for inhibition (C; SD = 0.4). D and E: population histograms showing that the majority of cells (88.5%) had negative GE response shifts (D, top left, 46/52 cells) and 94.5% of cells had negative GI response shifts (E, top left, 52/55 cells), regardless of binaural preference categorization.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Altshuler MW, Comalli PE. Effect of stimulus intensity and frequency on median horizontal plane sound localization. J Aud Res 15: 262–265, 1975
    1. Barry PH. JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. J Neurosci Methods 51: 107–116, 1994 - PubMed
    1. Campbell RA, Schnupp JW, Shial A, King AJ. Binaural-level functions in ferret auditory cortex: evidence for a continuous distribution of response properties. J Neurophysiol 95: 3742–3755, 2006a - PMC - PubMed
    1. Campbell RA, Doubell TP, Nodal FR, Schnupp JWH, King AJ. Interaural timing cues do not contribute to the map of space in the ferret superior colliculus: a virtual acoustic space study. J Neurophysiol 95: 242–254, 2006b - PubMed
    1. Chadderton P, Agapiou JP, McAlpine D, Margrie TW. The synaptic representation of sound source location in auditory cortex. J Neurosci 29: 14127–14135, 2009 - PMC - PubMed

Publication types

LinkOut - more resources