Development of complex sound representations in the primary auditory cortex

by

Michele Nerissa Insanally

Doctor of Philosophy in Neuroscience

University of California, Berkeley

Professor Shaowen Bao, PhD., Chair

The brain has a tremendous ability to change as a result of experience; this property is known as plasticity. Our mastery of soccer, rhetoric, agriculture and instrumentation are all learned skills that require experience. While the brain is plastic throughout life, during early development, the brain demonstrates a heightened sensitivity to experience. This unique epoch during development in which the brain is particularly susceptible to change is called a critical period. During the critical period, sensory experience results in significant modifications in structure and function. The set of studies described in this dissertation aim to investigate how complex sound representation develops during the critical period in the rat primary auditory cortex.

Previous examinations of the critical period in the auditory cortex have typically used simple tonal stimuli. Repeated exposure of rat pups to a tone, for instance, has been shown to selectively enlarge cortical representation of the tone and alter perceptual behaviors. However, probing cortical plasticity with a single-frequency tone might not reveal the full complexity and dynamics of critical period plasticity. After all, natural, biologically important sounds are generally complex with respect to their spectrotemporal properties. Natural sounds often have frequencies that vary in time and amplitude modulation. Psychophysical studies indicate that early experience of complex sounds has a profound impact on auditory perception and perceptual behaviors. Experience with speech, for instance, shapes language-specific phonemic perception, enhancing perceptual contrasts of native speech sounds and reducing perceptual contrasts of some foreign speech sounds. At the electrophysiological level, auditory cortical neurons preferentially respond to certain complex sounds, such as species-specific animal vocalizations. It is unclear how such selectivity for a complex sound emerges, and whether it is innate or shaped by early experience.

In order to address this question, we exposed rat pups to a frequency-modulated (FM) sweep in different time windows during early development, and examined the effects of such sensory experience on sound representations in the primary auditory cortex (AI). We found that early exposure to an FM sound resulted in altered characteristic frequency representations and broadened spectral tuning in AI neurons. In contrast, later exposure to the same sound only led to greater selectivity for the sweep rate and direction of the experienced FM sound. These results indicate that cortical representations of different acoustic features are shaped by complex sounds in a series of distinct critical periods.

Next, we confirmed this model of brain development in a set of experiments that examine how exposure to noise affects these various critical periods. We examined the influence of pulsed noise experience on the development of sound representations in AI. In naïve animals, FM sweep direction selectivity depends on the characteristic frequency (CF) of the neuron--low CF neurons tend to select for upward sweeps and high CF neurons for downward sweeps. Such a CF dependence was not observed in animals that had received weeklong exposure to pulsed noise in periods from postnatal day 8 (P8) to P15 or from P24 to P39. In addition, AI tonotopicity, tuning bandwidth, intensity threshold, tone-responsiveness, and sweep response magnitude were differentially affected by the noise experience depending on the exposure time windows. These results are consistent with previous findings of feature-dependent multiple sensitive periods. The different effects induced here by pulsed noise and previously by FM sweeps further indicate that plasticity in cortical complex sound representations is specific to the sensory input.

Identifying how the developing brain processes sensory information provides a foundation for understanding more complex behaviors. These results advance our understanding of the neuronal mechanisms underlying sensory development and language learning. Specifically, they elucidate the age-dependent effects of complex sound exposure on spectral tuning and complex sound representation in the rat primary auditory cortex. In addition, they provide a foundation for subsequent studies investigating the neural basis of language development.