The question of how sensory feedback shapes learned behavior is fundamental to understanding how we acquire and loose skills. In passerine birds such as zebra finches, song development and adult song maintenance critically depend on auditory feedback, and the study of these gives insight into the mechanisms for learning in the context of complex sensorimotor behaviors. Recent evidence highlights surprising state-dependent processing in the birdsong system, showing that the organization of the motor program during singing and the expression of auditory activity is regulated by the activity of the cholinergic basal forebrain (BF), including effects on HVc neurons. Using cellular, systems, and behavioral analysis, this project explores the role of behavioral state in sensorimotor learning in the birdsong system. The first experiment will characterize the role of BF in regulating singing. Singing behavior will be characterized after disruption of BF by lesion or electrical stimulation. BF manipulations will be combined with other lesions designed to manipulate auditory feedback, testing if BF contributes to feedback mediated learning. Single cell recordings during singing will provide insight into how compensatory responses including auditory feedback signals are transmitted throughout the song system. The second experiment will elucidate the synaptic mechanisms of cholinergic activity, manipulating both the cholinergic milieu and fictive output and auditory input in an in vitro brain slice preparation of HVc. Finally, cholinergic properties of HVc cells recorded in anesthetized birds will be assessed to relate the in vivo and in vitro results. Cholinergic activity has long been associated with states of heightened perceptual attention, but its role in sensorimotor learning has never been extensively analyzed. This project will test the hypothesis that cholinergic activity regulates sensorimotor learning. Positive results may also contribute to an understanding of the relation between basal forebrain degeneration and language disturbances in humans.

Agency
National Institute of Health (NIH)
Institute
National Institute of Mental Health (NIMH)
Type
Research Project (R01)
Project #
5R01MH059831-10
Application #
7559710
Study Section
Sensorimotor Integration Study Section (SMI)
Program Officer
Vicentic, Aleksandra
Project Start
1999-05-05
Project End
2010-12-31
Budget Start
2009-01-01
Budget End
2010-12-31
Support Year
10
Fiscal Year
2009
Total Cost
$316,743
Indirect Cost
Name
University of Chicago
Department
Biology
Type
Schools of Medicine
DUNS #
005421136
City
Chicago
State
IL
Country
United States
Zip Code
60637
Fukushima, Makoto; Rauske, Peter L; Margoliash, Daniel (2015) Temporal and rate code analysis of responses to low-frequency components in the bird's own song by song system neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol 201:1103-14
Fukushima, Makoto; Margoliash, Daniel (2015) The effects of delayed auditory feedback revealed by bone conduction microphone in adult zebra finches. Sci Rep 5:8800
Adret, Patrice; Meliza, C Daniel; Margoliash, Daniel (2012) Song tutoring in presinging zebra finch juveniles biases a small population of higher-order song-selective neurons toward the tutor song. J Neurophysiol 108:1977-87
Toth, Bryan A; Kostuk, Mark; Meliza, C Daniel et al. (2011) Dynamical estimation of neuron and network properties I: variational methods. Biol Cybern 105:217-37
Rauske, Peter L; Chi, Zhiyi; Dave, Amish S et al. (2010) Neuronal stability and drift across periods of sleep: premotor activity patterns in a vocal control nucleus of adult zebra finches. J Neurosci 30:2783-94
Margoliash, Daniel (2010) Sleep, learning, and birdsong. ILAR J 51:378-86
Shea, Stephen D; Koch, Henner; Baleckaitis, Daniel et al. (2010) Neuron-specific cholinergic modulation of a forebrain song control nucleus. J Neurophysiol 103:733-45
Shea, Stephen D; Margoliash, Daniel (2010) Behavioral state-dependent reconfiguration of song-related network activity and cholinergic systems. J Chem Neuroanat 39:132-40
Margoliash, Daniel; van Drongelen, Wim; Kohrman, Michael (2010) Introducing songbirds as a model system for epilepsy research. J Clin Neurophysiol 27:433-7
Brawn, Timothy P; Fenn, Kimberly M; Nusbaum, Howard C et al. (2010) Consolidating the effects of waking and sleep on motor-sequence learning. J Neurosci 30:13977-82

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