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The Journal of Neuroscience, May 6, 2009, 29(18):6013-6021; doi:10.1523/JNEUROSCI.5733-08.2009

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Behavioral/Systems/Cognitive
Entrainment of Slow Oscillations of Auditory Thalamic Neurons by Repetitive Sound Stimuli

Lixia Gao,¹ Xiankai Meng,² Changquan Ye,¹ Haitian Zhang,¹ Chunhua Liu,¹ Yang Dan,^3,4 Mu-ming Poo,^1,3 Jufang He,² and Xiaohui Zhang¹

¹Institute of Neuroscience, State Key Laboratory of Neuroscience, Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences, Shanghai 200031, China, ²Department of Rehabilitation Sciences, Hong Kong Polytechnic University, Hong Kong, China, and ³Division of Neurobiology, Department of Molecular and Cell Biology, Helen Wills Neuroscience Institute and ⁴Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, California 94720

Correspondence should be addressed to either of the following: Jufang He, Department of Rehabilitation Sciences, Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China, Email: Jufang.He{at}inet.polyu.edu.hk; or Xiaohui Zhang, Institute of Neuroscience, Chinese Academy of Sciences, 320 Yue-Yang Road, Shanghai 200031, China, Email: xhzhang{at}ion.ac.cn

Slow oscillations at frequencies <1 Hz manifest in many brain regions as discrete transitions between a depolarized up state and a hyperpolarized down state of the neuronal membrane potential. Although up and down states are known to differentially affect sensory-evoked responses, whether and how they are modulated by sensory stimuli are not well understood. In the present study, intracellular recording in anesthetized guinea pigs showed that membrane potentials of nonlemniscal auditory thalamic neurons exhibited spontaneous up/down transitions at random intervals in the range of 2–30 s, which could be entrained to a regular interval by repetitive sound stimuli. After termination of the entraining stimulation (ES), regular up/down transitions persisted for several cycles at the ES interval. Furthermore, the efficacy of weak sound stimuli in triggering the up-to-down transition was potentiated specifically at the ES interval for at least 10 min. Extracellular recordings in the auditory thalamus of unanesthetized guinea pigs also showed entrainment of slow oscillations by rhythmic sound stimuli during slow wave sleep. These results demonstrate a novel form of network plasticity, which could help to retain the information of stimulus interval on the order of seconds.

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Received Dec. 2, 2008; revised March 8, 2009; accepted April 2, 2009.

Correspondence should be addressed to either of the following: Jufang He, Department of Rehabilitation Sciences, Hong Kong Polytechnic University, Hung Hom, Kowloon, Hong Kong, China, Email: Jufang.He{at}inet.polyu.edu.hk; or Xiaohui Zhang, Institute of Neuroscience, Chinese Academy of Sciences, 320 Yue-Yang Road, Shanghai 200031, China, Email: xhzhang{at}ion.ac.cn

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