Postnatal Maturation of Primary Auditory Cortex in the Mustached Bat, Pteronotus parnellii

Abstract

mary auditory cortex (AI) of adult Pteronotus parnellii features a foveal representation of the second harmonic constant frequency (CF2) echolocation call component. In the corresponding Dopplershifted constant frequency (DSCF) area, the 61 kHz range is overrepresented for extraction of frequency-shift information in CF2 echoes. To assess to which degree AI postnatal maturation depends on active echolocation or/and reflects ongoing cochlear maturation, cortical neurons were recorded in juveniles up to postnatal day P29, before the bats are capable of active foraging. At P1-2, neurons in posterior AI are tuned sensitively to low frequencies (22-45 dB SPL, 28 -35 kHz). Within the prospective DSCF area, neurons had insensitive responses (Ͼ60 dB SPL) to frequencies Ͻ40 kHz and lacked sensitive tuning curve tips. Up to P10, when bats do not yet actively echolocate, tonotopy is further developed and DSCF neurons respond to frequencies of 51-57 kHz with maximum tuning sharpness (Q 10dB ) of 57. Between P11 and 20, the frequency representation in AI includes higher frequencies anterior and dorsal to the DSCF area. More multipeaked neurons (33%) are found than at older age. In the oldest group, DSCF neurons are tuned to frequencies close to 61 kHz with Q 10dB values Յ212, and threshold sensitivity, tuning sharpness and cortical latencies are adult-like. The data show that basic aspects of cortical tonotopy are established before the bats actively echolocate. Maturation of tonotopy, increase of tuning sharpness, and upward shift in the characteristic frequency of DSCF neurons appear to strongly reflect cochlear maturation.

Mechanisms of spectral and temporal integration in the mustached bat inferior colliculus

“…One explanation for the well-defined set of interactions underlying combination sensitivity is that the system appears to be prewired before the first experience with echolocation. Thus, tuning to pulse-echo delay occurs in the auditory cortex on the first day after birth, and many features of mature responses are evident within the first week (Vater et al, 2010; Kössl et al, 2012). It is not clear whether this tuning precedes combination sensitivity in the IC, but our hypothesis is that the brainstem and midbrain mechanisms and circuitry form during prenatal development.…”

Auditory cortex of newborn bats is prewired for echolocation

“…It is conspicuous that at the same developmental stage when delay-sensitive neurons are already functional, frequency tuning in the ventrally located primary AC is still quite immature because of ongoing inner ear development. In addition, other forms of facilitative combination sensitivity, reported for adult primary AC are still absent during the first postnatal week 20 . Therefore, one of the neuronal characteristics most crucial and advanced in terms of echolocation processing seems to appear first and not last in the maturation hierarchy of AC.…”

“…The age-related increase in sensitivity of involved cortical delay-tuned neurons, however, is most likely not dependent on experience but produced by maturation of the cochlea (PP: ref. 15) as it has been suggested for development of the primary AC of PP 20 . In the ascending auditory system, delay-sensitive neuronal responses are first created at the midbrain level (PP: refs 18,19).…”

“…PP cannot be bred in sufficient numbers in captivity and were caught in Cuban caves, experiments in 33 young bats and 13 adults took place at Havana University. Age was determined from forearm length 14,15,20 . Newborns have a forearm length of ~20 mm and the growth rate is ~1 mm per day.…”

“…Craniotomy was performed to expose small areas of the left AC. The location of auditory areas was determined from major blood vessels and, in the case of PP, from the Sylvian fissure and from published cortex maps on adults 3,4,37-39 and young bats 20 . After experiments, the animals were killed by Pentobarbital overdose and heads were preserved in 4% paraformaldehyde.…”