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The Journal of Neuroscience, March 9, 2005, 25(10):2490-2503; doi:10.1523/JNEUROSCI.5289-04.2005

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Behavioral/Systems/Cognitive
Plasticity in Primary Auditory Cortex of Monkeys with Altered Vocal Production

Steven W. Cheung,¹ Srikantan S. Nagarajan,² Christoph E. Schreiner,¹ Purvis H. Bedenbaugh,³ and Andrew Wong¹

¹Coleman Memorial Laboratory and W. M. Keck Center for Integrative Neuroscience, Department of Otolaryngology-Head and Neck Surgery, University of California, San Francisco, California 94143-0342, ²Department of Radiology, University of California, San Francisco, California 94143-0628, and ³Departments of Neuroscience and Otolaryngology, University of Florida Brain Institute, Gainesville, Florida 32610-0244

Response properties of primary auditory cortical neurons in the adult common marmoset monkey (Callithrix jacchus) were modified by extensive exposure to altered vocalizations that were self-generated and rehearsed frequently. A laryngeal apparatus modification procedure permanently lowered the frequency content of the native twitter call, a complex communication vocalization consisting of a series of frequency modulation (FM) sweeps. Monkeys vocalized shortly after this procedure and maintained voicing efforts until physiological evaluation 5-15 months later. The altered twitter calls improved over time, with FM sweeps approaching but never reaching the normal spectral range. Neurons with characteristic frequencies <4.3 kHz that had been weakly activated by native twitter calls were recruited to encode self-uttered altered twitter vocalizations. These neurons showed a decrease in response magnitude and an increase in temporal dispersion of response timing to twitter call and parametric FM stimuli but a normal response profile to pure tone stimuli. Tonotopic maps in voice-modified monkeys were not distorted. These findings suggest a previously unrecognized form of cortical plasticity that is specific to higher-order processes involved in the discrimination of more complex sounds, such as species-specific vocalizations.

Key words: auditory cortex; plasticity; primate; vocalization; learning; twitter call

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Received June 16, 2004; revised January 23, 2005; accepted January 23, 2005.

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