Enduring effects of early structured noise exposure on temporal modulation in the primary auditory cortex

Abstract

Studies have shown that acoustic experiences significantly contribute to the functional shaping of the structural organization and signal processing capacities of the mammalian auditory system during postnatal development. Here, we show how an early epoch of exposure to structured noise influences temporal processing in the rat primary auditory cortex documented immediately after exposure and again in adulthood. Pups were continuously exposed to broadband-pulsed noise across the critical period for auditory system development. Immediately after cessation of exposure at postnatal day Ϸ35 (P35) or Ϸ55 days later (i.e., P90) in other rats, the temporal modulation-transfer functions of cortical neurons were documented. We found that pulsed noise exposure at a low modulation rate significantly decreased cortical responses to repetitive stimuli presented across a range of higher modulation rates. The highest temporal rate at which temporal modulationtransfer function was at half of its maximum was reduced when compared with naïve rats. Low-rate pulsed noise exposure also decreased cortical response synchronization at higher stimulus rates, as shown by vector strength and Rayleigh statistic measures. These postexposure changes endured into adulthood. These findings bear significant implications for the role of early sound experiences as contributors to the ontogeny of human auditory and language-related abilities and impairments.cortical plasticity ͉ critical period ͉ temporal modulation-transfer function ͉ temporal processing S ounds in natural environments, such as animal vocalizations and human speech, have complex temporal structures. The importance of temporal structure in acoustic communication and orientation has been demonstrated in many behavioral, psychological, and neurophysiological studies. The auditory cortex plays a critical role in the perception of time-varying features of aural speech and of other complex acoustic stimuli. In humans, speech comprehension is correlated with responses of cortical neurons to temporal envelopes of speech (1), and individuals with impaired language abilities have impaired successive signal evoked cortical responses (2, 3).Earlier studies in different subprimate animal species have shown that cortical neurons display different temporal filtering properties (e.g., low-pass, responding to sound trains below certain rates, or band-pass, responding best to a specific rate, etc.) (4-7). In general, cortical neurons respond to repetitive sounds at far lower rates and with poorer temporal precision when compared with auditory nerve fibers or neurons in subcortical auditory nuclei and, in most mammalian species, are not able to follow individual sound presented at rates faster than Ϸ20 pulses per second (pps). It has been argued that for those more rapidly occurring stimuli (e.g., stimuli with repetition rate Ͼ100 pps), cortical neurons might apply a rate code instead of a temporal code (stimulus-synchronized responses) to represent the temporal structure (7). Most natural sounds, ...

Environmental Acoustic Enrichment Promotes Recovery from Developmentally Degraded Auditory Cortical Processing

“…Here we examined that effect by comparing the data obtained from the different rat groups. As shown in Figure 2D, values recorded in NE rats did not significantly differ from those of naive rats (ANOVA with post hoc Student-Newman-Keuls test, all p Ͼ 0.05), indicating that noise exposure has little effect on response thresholds of cortical neurons (Zhang et al, 2002;Zhou and Merzenich, 2008). Response thresholds recorded in AEE rats also were comparable to those of naive rats at low and high CF ranges (ANOVA with post hoc Student-Newman-Keuls test, both p Ͼ 0.05) but were lower at the middle CF range (ANOVA with post hoc Student-NewmanKeuls test, p Ͻ 0.01).…”

“…The overall boundaries of the A1 were functionally determined using nonresponsive sites and responsive sites that did not have a well defined pure tone-evoked response area (i.e., non-A1 sites; Merzenich, 2009, 2012). As previously described (Polley et al, 2006(Polley et al, , 2007Profant et al, 2013), A1 has a unique rostral-to-caudal tonotopy and reliable neuronal responses to tone pips of selective frequencies.…”

“…Rats used for immunohistochemistry were not those already used for behavioral testing or cortical recording but were otherwise treated in the same way. As in our earlier studies (de VillersSidani et al, 2010;Zhou and Merzenich, 2012), rats were deeply anesthetized with sodium pentobarbital (75 mg/kg body weight) and were perfused intracardially with saline solution followed by 4% paraformaldehyde in 0.1 M potassium PBS, pH 7.2. Brains were removed and placed in the same fixative containing 20% sucrose for 12-24 h. Fixed material was cut in the coronal plane on a freezing microtome at 40 m thickness.…”

“…Overlap index of frequency tuning curves was computed by first transforming the frequency tuning curves recorded from two cortical sites into 1D vectors and then calculating the peak of the normalized correlation coefficient between the two vectors produced (de Villers-Sidani et al, 2010;Zhou et al, 2011). Indices were obtained for all pairs of recording sites with various distances within a single animal.…”

The Medial Olivocochlear System Attenuates the Developmental Impact of Early Noise Exposure

“…For example, an early exposure to continuous white noise delays the emergence of adult tonotopic organization and frequency selectivity in auditory cortex (Chang and Merzenich 2003). An exposure to temporally modulated noise degrades stimulus entrainment (Zhou and Merzenich 2008;). An exposure to repeating transients disrupts stimulus following responses and frequency selectivity in the inferior colliculus (Sanes and Constantine-Paton 1985a, b).…”