Mechanisms of Sound Localization in Two Functionally Distinct Regions of the Auditory Cortex

Abstract

The auditory cortex is necessary for sound localization. The mechanisms that shape bicoordinate spatial representation in the auditory cortex remain unclear. Here, we addressed this issue by quantifying spatial receptive fields (SRFs) in two functionally distinct cortical regions in the pallid bat. The pallid bat uses echolocation for obstacle avoidance and listens to prey-generated noise to localize prey. Its cortex contains two segregated regions of response selectivity that serve echolocation and localization of prey-generated noise. The main aim of this study was to compare 2D SRFs between neurons in the noise-selective region (NSR) and the echolocation region [frequencymodulated sweep-selective region (FMSR)]. The data reveal the following major differences between these two regions: (1) compared with NSR neurons, SRF properties of FMSR neurons were more strongly dependent on sound level; (2) as a population, NSR neurons represent a broad region of contralateral space, while FMSR selectivity was focused near the midline at sound levels near threshold and expanded considerably with increasing sound levels; and (3) the SRF size and centroid elevation were correlated with the characteristic frequency in the NSR, but not the FMSR. These data suggest different mechanisms of sound localization for two different behaviors. Previously, we reported that azimuth is represented by predictable changes in the extent of activated cortex. The present data indicate how elevation constrains this activity pattern. These data suggest a novel model for bicoordinate spatial representation that is based on the extent of activated cortex resulting from the overlap of binaural and tonotopic maps.

Congruent representation of visual and acoustic space in the superior colliculus of the echolocating bat Phyllostomus discolor

“…It has been shown that not only the behavioural responses differ between active and passive hearing in these animals (Goerlitz et al ., ), but also the neural processing of sounds (Suga & Schlegel, ; Schuller, ). For the bat Antrozous pallidus, it was even suggested that actively and passively perceived sounds are processed in two parallel auditory pathways (Razak et al ., , ). Therefore, we assumed that in the bat's SC ‘active’ and ‘passive’ acoustic space may also not be equally represented.…”

“…In a recent study, Razak et al . () demonstrated that in the auditory cortex of the pallid bat ( Antrozous pallidus ) two sub‐regions exist, which encode the spatial position of noise and echoes, respectively, based on different sound cues. In the noise‐selective region interaural intensity differences and frequency selectivity are the primary cues for representation of 2D acoustic space, whereas, in the region selective for echo‐information encoding of spatial information is dependent on pinna directionality.…”

Adaptations for Substrate Gleaning in Bats: The Pallid Bat as a Case Study

“…These studies show that the 2D location representation in the auditory cortex is fundamentally different than in the midbrain [Razak and Fuzessery, 2002;Razak 2011Razak , 2012Razak , 2016Razak et al, 2015]. Pallid bats fly with their ears facing downwards (pinna parallel to ground) when foraging.…”

“…The FM sweep selective region (FMSR), like the ventral ICc, contains neurons with tuning > 25 kHz and responds selectively to the bandwidths, rates, and direction of FM sweeps in the echolocation call [Razak and Fuzessery, 2006;. The noise selective region (NSR), like the lateral ICc, contains neurons tuned < 35 kHz and responds selectively to noise with energy between 5 and 35 kHz [Razak 2011, Razak et al, 2015. Thus, the segregated functional organization observed in the IC is continued in the auditory cortex.…”

“…Only the EI cluster was examined in this study [Razak et al, 2015]. By recording responses to broadband noise presented from 55 speakers, 2 major trends emerged.…”