Expectations substantially influence perception, but the neural mechanisms underlying this influence are not fully understood. A prominent view is that sensory neurons encode prediction error with respect to expectations on upcoming sensory input. Although the encoding of prediction error has been previously demonstrated in the human auditory cortex (AC), previous studies often induced expectations using stimulus repetition, potentially confounding prediction error with neural habituation. These studies also measured AC as a single population, failing to consider possible predictive specializations of different AC fields. Moreover, the few studies that considered prediction error to stimuli other than pure tones yielded conflicting results. Here, we used functional magnetic resonance imaging (fMRI) to systematically investigate prediction error to subjective expectations in auditory cortical fields Te1.0, Te1.1, Te1.2, and Te3, and two types of stimuli: pure tones and frequency modulated (FM) sweeps. Our results show that prediction error is elicited with respect to the participants’ expectations independently of stimulus repetition and similarly expressed across auditory fields. Moreover, despite the radically different strategies underlying the decoding of pure tones and FM-sweeps, both stimulus modalities were encoded as prediction error in most fields of AC. Altogether, our results provide unequivocal evidence that predictive coding is the general encoding mechanism in AC.

A central issue in auditory research is how the auditory brain encodes complex stimuli. However, the process by which the auditory cortex interprets complex sounds during development and the extent to which cortical organization can be manipulated by complex stimulation is still undetermined. We have addressed this gap in the following three studies. First, we characterized the responses of cortical neurons in adult chinchillas to frequency-modulated (FM) stimulation. Next, we asked whether FM coding at the cortical level is innate or if its development is influenced by normal postnatal environmental experience. Finally, we investigated the effect of sustained neonatal FM sweep exposure on the development of cortical responses to tonal and FM stimuli. In our adult study, results indicated that >90% of sampled neurons were responsive to FM sweeps. The population preference was for upward FM sweeps and for medium to fast speeds ( 0.3 kHz/ms). Three types of temporal response patterns were observed: a single peak at sweep onset/offset (‘onset’) and a single peak (‘late’) or multiple peaks (‘burst’) during the sweep. ‘Late’ units expressed the highest direction and speed selectivity; ‘onset’ units were selective only for direction and ‘burst’ units were selective for neither direction nor speed. In our developmental study, our results showed a significant developmental increase in FM direction selectivity. However, FM speed selectivity appeared to be established early in development. In our developmental plasticity study, we hypothesized that constant FM exposure would increase the proportion of auditory neurons that are selectively responsive to the conditioning FM sweep. However, our results showed that while tonal response latencies increased after the exposure period, the conditioning stimulus had minimal effect on the FM direction preferences of cortical neurons and decreased overall neuronal FM speed selectivity. In conclusion, we suggest that chinchilla auditory cortical neurons are not uniquely activated by FM sounds but that FM responses are largely predictable based on how changing frequency stimuli interact with the receptive fields of these neurons. We also propose that the development of FM direction sensitivity is experience-independent and that perhaps normal acoustic experience is required to maintain FM speed tuning.

A central issue in auditory research is how the auditory brain encodes complex stimuli. However, the process by which the auditory cortex interprets complex sounds during development and the extent to which cortical organization can be manipulated by complex stimulation is still undetermined. We have addressed this gap in the following three studies. First, we characterized the responses of cortical neurons in adult chinchillas to frequency-modulated (FM) stimulation. Next, we asked whether FM coding at the cortical level is innate or if its development is influenced by normal postnatal environmental experience. Finally, we investigated the effect of sustained neonatal FM sweep exposure on the development of cortical responses to tonal and FM stimuli. In our adult study, results indicated that >90% of sampled neurons were responsive to FM sweeps. The population preference was for upward FM sweeps and for medium to fast speeds ( 0.3 kHz/ms). Three types of temporal response patterns were observed: a single peak at sweep onset/offset (‘onset’) and a single peak (‘late’) or multiple peaks (‘burst’) during the sweep. ‘Late’ units expressed the highest direction and speed selectivity; ‘onset’ units were selective only for direction and ‘burst’ units were selective for neither direction nor speed. In our developmental study, our results showed a significant developmental increase in FM direction selectivity. However, FM speed selectivity appeared to be established early in development. In our developmental plasticity study, we hypothesized that constant FM exposure would increase the proportion of auditory neurons that are selectively responsive to the conditioning FM sweep. However, our results showed that while tonal response latencies increased after the exposure period, the conditioning stimulus had minimal effect on the FM direction preferences of cortical neurons and decreased overall neuronal FM speed selectivity. In conclusion, we suggest that chinchilla auditory cortical neurons are not uniquely activated by FM sounds but that FM responses are largely predictable based on how changing frequency stimuli interact with the receptive fields of these neurons. We also propose that the development of FM direction sensitivity is experience-independent and that perhaps normal acoustic experience is required to maintain FM speed tuning.

Natural sound, such as conspecific vocalizations and human speech, represents an important part of the sensory signals animals and humans encounter in their daily lives. This dissertation investigates the neural mechanisms involved in creating response selectivity for complex features of natural acoustic signals and demonstrates that selectivity for spectral motion cues provides a neural mechanism to encode communication signals in the auditory midbrain. Spectral motion is defined as the movement of sound energy upward or downward in frequency at a certain velocity, and is believed to provide the auditory system with an important perceptual cue in the processing of human speech. Using the Mexican free-tailed bat, tadarida brasiliensis, as a model system, this research examined the role of selectivity for spectral motion cues, such as direction and velocity, in creating response selectivity for specific features of the social communication signals emitted by these animals. We show that auditory neurons in the midbrain nucleus of the inferior colliculus (IC) are specifically tuned for the frequency-modulated (FM) direction and velocities found in their conspecific vocalizations. This close agreement between neural tuning and features of natural conspecific signals shows that auditory neurons have evolved to specifically encode features of signals that are vital for the survival of the animal. Furthermore, we find that the neural computations resulting in selectivity for spectral motion are analogous to mechanisms observed in selectivity for visual motion, suggesting the evolution of similar neural mechanisms across sensory modalities. / text