Cortical circuits for dynamic auditory perception
The long-term goal of our research is to identify the neuronal circuits and neuronal codes that support hearing and auditory memory and learning in complex acoustic environments. Auditory perception is shaped by the interaction of sensory inputs with our experiences, emotions, and cognitive states. Decades of research have characterized how neuronal response properties to basic sounds, such as tones or whistles, are transformed in the auditory pathway of passively listening subjects. Much less well-understood is how the brain creates a perceptual representation of a complex auditory scene, i.e., one that is composed of a myriad of sounds, and how this representation is shaped by learning and experience. Over the last six years, our laboratory has made transformative progress in the quantitative understanding of neuronal circuits supporting dynamic auditory perception, through a combination of behavioral, electrophysiological, optogenetic and computational approaches. Specifically, we have:
(1) Discovered a novel role for the auditory cortex in learning-driven changes in auditory acuity;
(2) Discovered a novel intra-cortical circuit supporting adaptation to temporal regularities in sounds;
(3) Identified computational mechanisms for encoding of complex sounds in the auditory cortex;
(4) Identified neural mechanisms underlying development of perception of environmental sounds and speech perception.
With these findings, our laboratory is positioned to make a breakthrough in the computational and theoretical understanding of audition over the next few years. Whereas the specific research projects in the laboratory focus on investigating distinct circuits involved in specific auditory functions, our aspiration is to develop a comprehensive computational framework for understanding neuronal dynamics in perception and memory. Our focus on the function these circuits in audition will pave the way for understanding processing across sensory modalities and brain regions.
NEURONAL CIRCUITS FACILITATING HEARING IN COMPLEX ACOUSTIC ENVIRONMENTS
Adaptation to stimulus context is a ubiquitous property of cortical neurons, thought to enhance efficiency of sensory coding. Yet the specific neuronal circuits that facilitate cortical adaptation remain unknown. In the primary auditory cortex, the vast majority of neurons exhibit stimulus-specific adaptation, responding weakly to frequently repeated tones and strongly to rare tones. We are investigating the hypothesis that a complex circuit composed of several subtypes of cortical interneurons facilitates stimulus-specific adaptation. We use optogenetic methods to up-or down- regulate the activity of parvalbumin-positive or somatostatin-positive interneurons and test the effect of their manipulation on responses of principal cortical neurons. By reducing responses to frequent sounds, complex inhibitory networks may enhance cortical sensitivity to rare sounds that may represent unexpected events.
CORTICAL MECHANISMS DRIVING CHANGES IN AUDITORY PERCEPTION FOLLOWING EMOTIONAL LEARNING
Traumatic events lead to changes in the emotional response to the environment, and to changes in the way the environment is perceives. Identifying the brain circuits that link emotional responses and sensory perception is of crucial importance to learning the causes and developing treatments for anxiety and post-traumatic stress disorder (PTSD). We recently discovered a new link between emotional learning, a model of anxiety acquisition, and changes in perceptual acuity, and found that the auditory cortex plays a crucial in facilitating this plasticity. We are presently investigating the neuronal mechanisms that support dynamic changes in sensory perception driven by emotional learning, as well as identifying the source for individual variability in specificity of emotional learning. In order to achieve that, we combine behavioral, electrophysiological, computational and optogenetic tools. Our results will shed light on the circuits that are likely disrupted in PTSD and anxiety disorders and will eventually lead to development of novel tools for prevention and treatment of these devastating mental conditions.
SPECIALIZATION OF THE AUDITORY CORTEX FOR PROCESSING OF NATURAL SOUNDS
Sensory systems are thought to have evolved to efficiently encode and represent the full range of sensory stimuli encountered in the natural world. The statistics of natural environmental sounds have an intricate spectro-temporal structure, yet how populations of neurons encode and process information about such complex statistics is only beginning to be elucidated. We recently identified a new form of statistical dependence in environmental sounds: In sounds of running water, a subset of environmental sounds, the temporal modulation spectrum across spectral bands scales with the center frequency of the band. In a psychophysical study, we found that sounds that obeyed the invariant scaling relation, but which varied in cyclo-temporal coefficients and spectro-temporal sound density evoked different percepts, ranging from pattering of rain to sound of a waterfall to artificial ringing. We are presently exploring changing spectro-temporal statistical properties of water-like sounds affects responses of neurons in the primary auditory cortex.
An essential task of the auditory system is to tell apart different communication signals, such as vocalizations. We recently found that neuronal populations in the auditory cortex are specialized for encoding con-specific vocalizations. We are presently investigating the neuronal mechanisms for creating an invariant representation of vocalizations in the auditory pathways, which would allow the brain to preserve the ability to tell apart vocalizations produced by different speakers or in the presence of noise. We are testing the hypothesis that invariant representations are created gradually through hierarchical transformation within the auditory pathway.
COMPUTATION IN THE AUDITORY SYSTEM
Throughout our studies we combine electrophysiological investigation of the neuronal pathways with computational approaches. Our goal is to understand the principles of encoding of information by populations of neurons, the function of specific cortical circuits comprised of inhibitory and excitatory neurons in learning and perception, and the mechanisms driving development of auditory perception and speech comprehension