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The Journal of Neuroscience, December 10, 2008, 28(50):13629-13639; doi:10.1523/JNEUROSCI.4429-08.2008

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Behavioral/Systems/Cognitive
Stimulus-Timing-Dependent Plasticity of Cortical Frequency Representation

Johannes C. Dahmen, Douglas E. H. Hartley, and Andrew J. King

Department of Physiology, Anatomy and Genetics, University of Oxford, Oxford OX1 3PT, United Kingdom

Correspondence should be addressed to Dr. Andrew J. King, Department of Physiology, Anatomy and Genetics, Sherrington Building, University of Oxford, Parks Road, Oxford OX1 3PT, UK. Email: andrew.king{at}dpag.ox.ac.uk

Adult cortical circuits possess considerable plasticity, which can be induced by modifying their inputs. One mechanism proposed to underlie changes in neuronal responses is spike-timing-dependent plasticity (STDP), an up- or downregulation of synaptic efficacy contingent upon the order and timing of presynaptic and postsynaptic activity. The repetitive and asynchronous pairing of a sensory stimulus with either another sensory stimulus or current injection can alter the response properties of visual and somatosensory neurons in a manner consistent with STDP. To examine whether such plasticity also exists in the auditory system, we recorded from neurons in the primary auditory cortex of anesthetized and awake adult ferrets. The repetitive pairing of pure tones of different frequencies induced shifts in neuronal frequency selectivity, which exhibited a temporal specificity akin to STDP. Only pairs with stimulus onset asynchronies of 8 or 12 ms were effective and the direction of the shifts depended upon the order in which the tones within a pair were presented. Six hundred stimulus pairs (lasting ~70 s) were enough to produce a significant shift in frequency tuning and the changes persisted for several minutes. The magnitude of the observed shifts was largest when the frequency separation of the conditioning stimuli was < ~1 octave. Moreover, significant shifts were found only in the upper cortical layers. Our findings highlight the importance of millisecond-scale timing of sensory input in shaping neural function and strongly suggest STDP as a relevant mechanism for plasticity in the mature auditory system.

Key words: auditory cortex; ferret; sound frequency tuning; spike-timing-dependent plasticity; conditioning; sound

Received Sept. 16, 2008; revised Nov. 6, 2008; accepted Nov. 7, 2008.

Correspondence should be addressed to Dr. Andrew J. King, Department of Physiology, Anatomy and Genetics, Sherrington Building, University of Oxford, Parks Road, Oxford OX1 3PT, UK. Email: andrew.king{at}dpag.ox.ac.uk






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