The brain must filter the overwhelming influx of sensory information to select information that is relevant to its current goals, in order to appropriately guide adaptive behavior. While studies in macaque monkeys have identified many of the mechanisms underlying attention effects on visual processing, very few studies have examined corresponding effects in the auditory system. Recent findings raise our overarching hypothesis that attention enhances the sensory representation of attended stimuli at the expense of ignored ones both by modulating local excitability within, and the dynamic routing of information across distinct functional areas in the brain. The broad goal of the proposed research is to examine this hypothesis and thus define the mechanisms of these interrelated local and network based processes, as well as their relative contributions to attentive auditory stimulus processing in different nodes of the auditory processing hierarchy. According to our hypothesis, attention modulates ongoing oscillatory activity to match its properties (frequency and phase) to the global acoustic features of the attended stimulus stream (temporal structure and pitch respectively), thereby creating an internal model of that stream in the form of subthreshold neuronal oscillations. This allows the oscillations to act as a template-based filter mechanism that segregates the relevant stream and enhances its processing along fundamental organizing dimensions of auditory objects. Parallel to this, the alignment of oscillatory activity across hierarchical processing stages biases the transmission of relevant information by providing a common temporal reference frame for communication that is tied to the temporal structure of the attended auditory stream. A key to both local enhancement and network based communication effects is the alignment of oscillatory phase to the timing of relevant events by oscillatory phase reset. Converging evidence suggests that phase reset is initiated by direct non-lemniscal thalamocortical afferents, and is modulated by top-down attention via the reticular nucleus of the thalamus. Our first specific aim is to determine the set of rules that define the way ambient subthreshold activity in primary auditory cortex is modulated by attention and by the physical properties of auditory stimulus streams. Our second specific aim is to define the mechanism and determine the role of attention related changes in functional connectivity between primary and higher level belt regions of auditory cortex. Our third specific aim is to identify the thalamic structures that initiate and modulate oscillatory phse reset by analyzing the concurrent electrophysiological activity of auditory thalamic and primary cortical regions, and using electrical microstimulation. The application of paired recordings across different nodes of the auditory thalamocortical processing hierarchy will provide fundamental information on how dynamic brain networks function, and are modulated by attention. This will allow for a direct mechanistic interpretation of auditory perceptual and attention related deficits, which are hallmark symptoms of many debilitating neuropsychiatric disorders.

Public Health Relevance

Describing the mechanisms that modulate and dynamically route information during attentive auditory perceptual processes will improve our understanding on how the brain accomplishes the task of segregating and selecting relevant items from the overwhelming influx of sensory information. This constitutes an important step towards developing a dynamic model of perceptual/cognitive impairments that are frequently occurring among the symptoms of many neuropsychiatric disorders, most notably schizophrenia, attention-deficit hyperactivity disorder and autism.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
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Mechanisms of Sensory, Perceptual, and Cognitive Processes Study Section (SPC)
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Platt, Christopher
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Nathan Kline Institute for Psychiatric Research
United States
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Barczak, Annamaria; O'Connell, Monica Noelle; McGinnis, Tammy et al. (2018) Top-down, contextual entrainment of neuronal oscillations in the auditory thalamocortical circuit. Proc Natl Acad Sci U S A 115:E7605-E7614
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