Development of functional organization of the pallid bat auditory cortex

Abstract

The primary auditory cortex is characterized by a tonotopic map and a clustered organization of binaural properties. The factors involved in the development of overlain representation of these two properties are unclear. We addressed this issue in the auditory cortex of the pallid bat. The adult pallid bat cortex contains a systematic relationship between best frequency (BF) and binaural properties. Most neurons with BF<30 kHz are binaurally inhibited (EO/I), while most neurons with BF>30 kHz are monaural (EO). As in other species, binaural properties are clustered. The EO/I cluster contains a systematic map of interaural intensity difference (IID) sensitivity. We asked if these properties are present at the time the bat acquires its full audible range (postnatal day [P] 15). Tonotopy, relationship between BF and binaural properties, and the map of IID sensitivity are adult-like at P15. However, binaural facilitation is only observed in pups older than P25. Frequency selectivity shows a BF-dependent sharpening during development. Thus, overlain representation of binaural properties and tonotopy in the pallid bat cortex is remarkably adult-like at an age when the full audible range is first present, suggesting an experience-independent development of overlapping feature maps.

Monaural Deprivation Disrupts Development of Binaural Selectivity in Auditory Midbrain and Cortex

“…The preservation of low frequency hearing induced an expansion of low frequency areas of the tonotopic map, but only in animals ligated at 2wks, in agreement with recent studies in the rat demonstrating that passive experience with spectrally modified sound environments only modifies the tonotopic map within the first few days after hearing onset (de Villers-Sidani et al, 2007; Insanally et al, 2009). Similar to binocular tuning in V1, binaural selectivity in AI emerges progressively over the first month of hearing (Razak and Fuzessery, 2007), as one would expect from the delay of organized connectivity for binaural versus topographic circuits in the developing auditory brainstem (Green and Sanes, 2005; Kim and Kandler, 2003). By demonstrating that ipsilateral augmentation is observed in rats ligated at 2wks or 4wks, but not in adulthood, our data confirm the prediction that interaural balance, like frequency modulation direction tuning, is shaped during a critical period extending into later postnatal development.…”

Exploiting Development to Evaluate Auditory Encoding of Amplitude Modulation

“…Furthermore, temporal discrimination is accompanied by activation of left ACx, and is impaired by ACx ablation or inactivation (Elliott and Trahiotis, 1972; Ohl et al, 1999). Additionally, although many studies have characterized the maturation of ACx processing (Eggermont, 1991; Bonham et al, 2004; Pienkowski and Harrison, 2005; Razak and Fuzessery, 2007b; Brown and Harrison, 2010), all employed anesthetized preparations, yielding data that might differ significantly from awake recordings, especially in ACx (Gaese and Ostwald, 2001; Wang et al, 2005). …”

Life history constrains biochemical development in the highly specialized odontocete echolocation system

“…Thus dolphins and porpoises are clearly able to produce high-frequency sounds at early stages of life, but the relative hearing capabilities of these young animals are unknown. The other group of echolocating mammals (bats) has functional binaural hearing by 25 days post partum (Razak & Fusessery 2007); however the sound reception mechanisms used by bats are completely different from those of odontocetes, making it difficult to generalize across echolocators.…”