Computational Analysis of Functional Imaging in the Primary Auditory Cortex

Functional imaging can reveal detailed organizational structure in cerebral cortical areas, but neuronal response features and local neural interconnectivity can influence the resulting images, possibly limiting the inferences that can be drawn about neural function. Historically, discerning the fundamental principles of organizational structure in the auditory cortex of multiple species has been somewhat challenging with functional imaging as the studies have failed to reproduce results seen in electrophysiology. One difference might result from the way most functional imaging studies record the summed activity of multiple neurons. To test this effect, virtual mapping experiments were run in order to gauge the ability of functional imaging to accurately estimate underlying maps. The experiments suggest that spatial averaging improves the ability to estimate maps with low spatial frequencies or with large amounts of cortical variability, at the cost of decreasing the spatial resolution of the images. Despite the decrease in resolution, the results suggest that current functional imaging studies may be able to depict maps with high spatial frequencies better than electrophysiology can; therefore, the difficulties in recapitulating electrophysiology experiments with imaging may stem from underlying neural circuitry. One possible reason may be the relative distribution of response selectivity throughout the population of auditory cortex neurons. A small percent of neurons have a response type that exhibits a receptive field size that increases with higher stimulus intensities, but they are likely to contribute disproportionately to the activity detected in functional images, especially if intense sounds are used for stimulation. To evaluate the potential influence of neuronal subpopulations upon functional images of the primary auditory cortex, a model array representing cortical neurons was probed with virtual imaging experiments under various assumptions about the local circuit organization. As expected, different neuronal subpopulations were activated preferentially under different stimulus conditions. In fact, stimulus protocols that can preferentially excite one subpopulation of neurons over the others have the potential to improve the effective resolution of functional auditory cortical images. These experimental results also make predictions about auditory cortex organization that can be tested with refined functional imaging experiments

Feature Topography and Sound Intensity Level Encoding in Primary Auditory Cortex

The primary auditory cortex: A1) in mammals is one of the first areas in the neocortex that receives auditory related spiking activity from the thalamus. Because the neocortex is implicated in regulating high-level brain phenomena, such as attention and perception, it is therefore important in regards to these high-level behaviors to understand how sounds are represented and transformed by neuronal circuits in this area. The topographic organization of neuronal responses to auditory features in A1 provides evidence for potential mechanisms and functional roles of this neural circuitry. This dissertation presents results from models of topographic organization supporting the notion that if the topographic organization of frequency responses, termed tonotopy or cochleotopy, is aligned along the longest anatomical line segment in A1, as supported by some physiological studies, then it is unlikely that any other topography is mapped monotonically along the orthogonal axis. Thresholds of neuronal responses to sound intensity level represent a particular feature that may have a local, highly periodic topography and that is vital to the sensitivity of the auditory system. The neuronal representation of sound level in A1, particularly as it relates to encoding accuracy, contains a distribution of neurons with varying amounts of inhibition at high sound levels. Neurons with large amounts of this high-level inhibition are described as nonmonotonic or level-tuned. This dissertation presents evidence from single neuron recordings in A1 that neurons exhibiting greater high-level inhibition also exhibit lower neuronal thresholds and that lower thresholds in these nonmonotonic neurons are preserved even when much of the neuronal population is adapted for accurately encoding more intense sounds. Evidence presented in this dissertation also suggests that nonmonotonic neurons have transient responses to time-varying: dynamic) level stimuli that adapt more quickly in response to low-level sounds than those of monotonic neurons. Together these results imply that under static, steady-state-dynamic and transient-dynamic sound level conditions, nonmonotonic neurons are specialized encoders of less intense sounds that allow the auditory system to maintain sensitivity under a variety of environmental conditions

A Map of Periodicity Orthogonal to Frequency Representation in the Cat Auditory Cortex

Harmonic sounds, such as voiced speech sounds and many animal communication signals, are characterized by a pitch related to the periodicity of their envelopes. While frequency information is extracted by mechanical filtering of the cochlea, periodicity information is analyzed by temporal filter mechanisms in the brainstem. In the mammalian auditory midbrain envelope periodicity is represented in maps orthogonal to the representation of sound frequency. However, how periodicity is represented across the cortical surface of primary auditory cortex (AI) remains controversial. Using optical recording of intrinsic signals, we here demonstrate that a periodicity map exists in primary AI of the cat. While pure tone stimulation confirmed the well-known frequency gradient along the rostro-caudal axis of AI, stimulation with harmonic sounds revealed segregated bands of activation, indicating spatially localized preferences to specific periodicities along a dorso-ventral axis, nearly orthogonal to the tonotopic gradient. Analysis of the response locations revealed an average gradient of − 100° ± 10° for the periodotopic, and −12° ± 18° for the tonotopic map resulting in a mean angle difference of 88°. The gradients were 0.65 ± 0.08 mm/octave for periodotopy and 1.07 ± 0.16 mm/octave for tonotopy indicating that more cortical territory is devoted to the representation of an octave along the tonotopic than along the periodotopic gradient. Our results suggest that the fundamental importance of pitch, as evident in human perception, is also reflected in the layout of cortical maps and that the orthogonal spatial organization of frequency and periodicity might be a more general cortical organization principle