Neuronal sensitivity to interaural time differences in the sound envelope in the auditory cortex of the pallid bat

A consistent organizational feature of auditory cortex is a clustered representation of binaural properties. Here we address two questions. What is the intrinsic organization of binaural clusters and to what extent does intracortical processing contribute to binaural representation. We address these issues in the auditory cortex of the pallid bat. The pallid bat listens to prey-generated noise transients to localize and hunt terrestrial prey. As in other species studied, binaural clusters are present in the auditory cortex of the pallid bat. One cluster contains neurons that require binaural stimulation to be maximally excited, and are commonly termed predominantly binaural (PB) neurons. These neurons do not respond to monaural stimulation of either ear but show a peaked sensitivity to interaural intensity differences (IID) centered near 0 dB IID. We show that the peak IID varies systematically within this cluster. The peak IID is also correlated with the best frequency (BF) of neurons within this cluster. In addition, the IID selectivity of PB neurons is shaped by intracortical GABAergic input. Iontophoresis of GABAA receptor antagonists on PB neurons converts a majority of them to binaurally inhibited (EI) neurons that respond best to sounds favoring the contralateral ear. These data indicate that the cortex does not simply inherit binaural properties from lower levels but instead sharpens them locally through intracortical inhibition. The IID selectivity of the PB cluster indicates that the pallid bat cortex contains an increased representation of the frontal space that may underlie increased localization accuracy in this region.

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GABA Shapes Selectivity for the Rate and Direction of Frequency-Modulated Sweeps in the Auditory Cortex

Journal of Neurophysiology ◽

10.1152/jn.00334.2009 ◽

2009 ◽

Vol 102 (3) ◽

pp. 1366-1378 ◽

Cited By ~ 44

Author(s):

Khaleel A. Razak ◽

Zoltan M. Fuzessery

Keyword(s):

Auditory Cortex ◽

Gabaa Receptor ◽

Gabaa Receptors ◽

High Frequency ◽

Arrival Time ◽

Low Frequency ◽

Direction Selectivity ◽

Similar Response ◽

Cortical Level ◽

Pallid Bat

In the pallid bat auditory cortex and inferior colliculus (IC), the majority of neurons tuned in the echolocation range is selective for the direction and rate of frequency-modulated (FM) sweeps used in echolocation. Such selectivity is shaped mainly by spectrotemporal asymmetries in sideband inhibition. An early-arriving, low-frequency inhibition (LFI) shapes direction selectivity. A delayed, high-frequency inhibition (HFI) shapes rate selectivity for downward sweeps. Using iontophoretic blockade of GABAa receptors, we show that cortical FM sweep selectivity is at least partially shaped locally. GABAa receptor antagonists, bicuculline or gabazine, reduced or eliminated direction and rate selectivity in ∼50% of neurons. Intracortical GABA shapes FM sweep selectivity by either creating the underlying sideband inhibition or by advancing the arrival time of inhibition relative to excitation. Given that FM sweep selectivity and asymmetries in sideband inhibition are already present in the IC, these data suggest a refinement or recreation of similar response properties at the cortical level.

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Functional Organization of the Pallid Bat Auditory Cortex: Emphasis on Binaural Organization

Journal of Neurophysiology ◽

10.1152/jn.00226.2001 ◽

2002 ◽

Vol 87 (1) ◽

pp. 72-86 ◽

Cited By ~ 39

Author(s):

Khaleel A. Razak ◽

Zoltan M. Fuzessery

Keyword(s):

Auditory Cortex ◽

Sound Localization ◽

High Frequency ◽

Functional Organization ◽

Low Frequency ◽

Frequency Region ◽

Broadband Noise ◽

Intensity Difference ◽

Band Pass ◽

Pallid Bat

This report maps the organization of the primary auditory cortex of the pallid bat in terms of frequency tuning, selectivity for behaviorally relevant sounds, and interaural intensity difference (IID) sensitivity. The pallid bat is unusual in that it localizes terrestrial prey by passively listening to prey-generated noise transients (1–20 kHz), while reserving high-frequency (<30 kHz) echolocation for obstacle avoidance. The functional organization of its auditory cortex reflects the need for specializations in echolocation and passive sound localization. Best frequencies were arranged tonotopically with a general increase in the caudolateral to rostromedial direction. Frequencies between 24 and 32 kHz were under-represented, resulting in hypertrophy of frequencies relevant for prey localization and echolocation. Most neurons (83%) tuned <30 kHz responded preferentially to broadband or band-pass noise over single tones. Most neurons (62%) tuned >30 kHz responded selectively or exclusively to the 60- to 30-kHz downward frequency-modulated (FM) sweep used for echolocation. Within the low-frequency region, neurons were placed in two groups that occurred in two separate clusters: those selective for low- or high-frequency band-pass noise and suppressed by broadband noise, and neurons that showed no preference for band-pass noise over broadband noise. Neurons were organized in homogeneous clusters with respect to their binaural response properties. The distribution of binaural properties differed in the noise- and FM sweep-preferring regions, suggesting task-dependent differences in binaural processing. The low-frequency region was dominated by a large cluster of binaurally inhibited neurons with a smaller cluster of neurons with mixed binaural interactions. The FM sweep-selective region was dominated by neurons with mixed binaural interactions or monaural neurons. Finally, this report describes a cortical substrate for systematic representation of a spatial cue, IIDs, in the low-frequency region. This substrate may underlie a population code for sound localization based on a systematic shift in the distribution of activity across the cortex with sound source location.

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