A critical period for the recovery of sound localization accuracy following monaural occlusion in the barn owl

Abstract

We studied the ability of barn owls to recover accurate sound localization after being raised with one ear occluded. Most of the owls had ear plugs inserted before they reached adult size, and therefore they never experienced normal adult localization cues until their ear plugs were removed. Upon removal of their ear plugs, these owls exhibited large systematic sound localization errors. The rate at which they recovered accurate localization decreased with the age of the bird at the time of plug removal, and recovery essentially ceased when owls reached 38 to 42 weeks of age. We interpret this age as the end of a critical period for the consolidation of associations between auditory cues and locations in space. Owls that had experienced adult localization cues for a short period of time before ear plugging recovered normal accuracy rapidly, even if they remained plugged well past the end of the critical period. This suggests that a brief exposure to normal adult cues early in the critical period is sufficient to enable the recovery of localization accuracy much later in life.

Concurrent Development of the Head and Pinnae and the Acoustical Cues to Sound Location in a Precocious Species, the Chinchilla (Chinchilla lanigera)

“…Chinchillas are also widely used for experimentally induced otitis media research (Margolis et al 1995;Giebink 1999). Aside from studies in the cat (Moore and Irvine 1979;Tollin and Koka 2009a, b), ferret (Schnupp et al 2003), and barn owl (Knudsen et al 1984a;Knudsen et al 1984b), there have been few studies on the development of the physical dimensions of the head and pinna and the changes in the resulting localization cues.…”

Sustained Perceptual Deficits from Transient Sensory Deprivation

“…Several previous findings support the notion that central auditory encoding is sensitive to critical period deprivation, yet they focus largely on monaural manipulations and their effect on binaural processing. In a series of important experiments, Knudsen and colleagues found that animals that are unilaterally earplugged before the age of P60 adapt to the plug both behaviorally and neurally, whereas animals that are plugged after P60 show no evidence of adaptation (Knudsen et al, 1982(Knudsen et al, , 1984bKnudsen, 1983Knudsen, , 1985Mogdans and Knudsen, 1992. Complementary results have been obtained in several species, leading to the conclusion that the central mechanisms underlying binaural perception depend on early auditory experience (Clements and Kelly, 1978;Moore and Irvine, 1981;King et al, 1988;Wilmington et al, 1994;Moore et al, 1999;King et al, 2000;Kacelnik et al, 2006;Popescu and Polley, 2010;Keating et al, 2013Keating et al, , 2015Polley et al, 2013;Tomlin and Rance, 2014).…”

“…This result is consistent with previous findings suggesting that juvenile perceptual deficits can resolve with additional maturation. For example, barn owls reared with a unilateral earplug demonstrate impaired sound localization immediately following the removal of the plug, but performance can improve to normal levels over time (Knudsen et al, 1982(Knudsen et al, , 1984a. Similarly, children with a history of otitis media display deficits in binaural hearing (Moore et al, 1991;Pillsbury et al, 1991;Hall et al, 1995;Hogan et al, 1996;Hall et al, 1998) and speech processing (Jerger and Johnson, 1988;Gravel and Wallace, 1992;Gravel et al, 1996;Hall et al, 2003) that gradually recover after normal peripheral audibility is restored.…”

A Sensitive Period for the Impact of Hearing Loss on Auditory Perception

“…In fact, children with chronic otitis media often experience transient hearing loss without damage to the cochlea and this deprivation is thought to impair neural and perceptual development (Whitton and Polley, 2011). Furthermore, unilateral CHL during development can impair binaural processing and speech detection in noise (Clements and Kelly, 1978;Knudsen et al, 1984aKnudsen et al, , 1984bMoore et al, 1999;Parsons et al, 1999;King et al, 2000). Longer durations of unilateral CHL, due to the congenital absence of an ear canal, are associated with a poorer ability to understand speech in the presence of noise after corrective surgery, suggesting termination of the sensitive period for recovery (Gray et al, 2009).…”

“…However, prolonged periods of conductive hearing loss (CHL) due to chronic otitis media may also induce perceptual deficits (Whitton and Polley, 2011). In fact, the central encoding of spatial location is profoundly altered by unilateral CHL and these functional changes can account for impaired perceptual abilities (Clements and Kelly, 1978;Knudsen et al, 1984aKnudsen et al, , 1984bWilmington et al, 1994;Moore et al, 1999;Parsons et al, 1999;King et al, 2000;Popescu and Polley, 2010). Furthermore, direct measures from auditory cortex demonstrate that CHL induced at the time of ear canal opening disrupts synapse function, but not when induced in adulthood (Takesian et al, 2012).…”