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The Journal of Neuroscience, December 31, 2008, 28(53):14467-14480; doi:10.1523/JNEUROSCI.3086-08.2008

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Behavioral/Systems/Cognitive
Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Elias B. Issa and Xiaoqin Wang

Laboratory of Auditory Neurophysiology, Department of Biomedical Engineering, Johns Hopkins University School of Medicine, Baltimore, Maryland 21025

Correspondence should be addressed to Xiaoqin Wang, Laboratory of Auditory Neurophysiology, Department of Biomedical Engineering, Johns Hopkins University School of Medicine, 720 Rutland Avenue, Traylor 410, Baltimore, MD 21205. Email: xiaoqin.wang{at}jhu.edu

Most sensory stimuli do not reach conscious perception during sleep. It has been thought that the thalamus prevents the relay of sensory information to cortex during sleep, but the consequences for cortical responses to sensory signals in this physiological state remain unclear. We recorded from two auditory cortical areas downstream of the thalamus in naturally sleeping marmoset monkeys. Single neurons in primary auditory cortex either increased or decreased their responses during sleep compared with wakefulness. In lateral belt, a secondary auditory cortical area, the response modulation was also bidirectional and showed no clear systematic depressive effect of sleep. When averaged across neurons, sound-evoked activity in these two auditory cortical areas was surprisingly well preserved during sleep. Neural responses to acoustic stimulation were present during both slow-wave and rapid-eye movement sleep, were repeatedly observed over multiple sleep cycles, and demonstrated similar discharge patterns to the responses recorded during wakefulness in the same neuron. Our results suggest that the thalamus is not as effective a gate for the flow of sensory information as previously thought. At the cortical stage, a novel pattern of activation/deactivation appears across neurons. Because the neural signal reaches as far as secondary auditory cortex, this leaves open the possibility of altered sensory processing of auditory information during sleep.

Key words: auditory cortex; lateral belt; sleep; primate; sensory; hearing

Received July 2, 2008; revised Oct. 24, 2008; accepted Nov. 14, 2008.

Correspondence should be addressed to Xiaoqin Wang, Laboratory of Auditory Neurophysiology, Department of Biomedical Engineering, Johns Hopkins University School of Medicine, 720 Rutland Avenue, Traylor 410, Baltimore, MD 21205. Email: xiaoqin.wang{at}jhu.edu






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