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The Journal of Neuroscience, May 7, 2008, 28(19):5040-5052; doi:10.1523/JNEUROSCI.5059-07.2008

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Behavioral/Systems/Cognitive
Spikes and Bursts in Two Types of Thalamic Projection Neurons Differentially Shape Sleep Patterns and Auditory Responses in a Songbird

Richard H. R. Hahnloser, Claude Z.-H. Wang, Aymeric Nager, and Katja Naie

Institute of Neuroinformatics, University of Zurich/Swiss Federal Institute of Technology Zurich, 8057 Zurich, Switzerland

Correspondence should be addressed to Richard H. R. Hahnloser, Institute of Neuroinformatics, University of Zurich/Swiss Federal Institute of Technology Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland. Email: rich{at}ini.phys.ethz.ch

In mammals, the thalamus plays important roles for cortical processing, such as relay of sensory information and induction of rhythmical firing during sleep. In neurons of the avian cerebrum, in analogy with cortical up and down states, complex patterns of regular-spiking and dense-bursting modes are frequently observed during sleep. However, the roles of thalamic inputs for shaping these firing modes are largely unknown. A suspected key player is the avian thalamic nucleus uvaeformis (Uva). Uva is innervated by polysensory input, receives indirect cerebral feedback via the midbrain, and projects to the cerebrum via two distinct pathways. Using pharmacological manipulation, electrical stimulation, and extracellular recordings of Uva projection neurons, we study the involvement of Uva in zebra finches for the generation of spontaneous activity and auditory responses in premotor area HVC (used as a proper name) and the downstream robust nucleus of the arcopallium (RA). In awake and sleeping birds, we find that single Uva spikes suppress and spike bursts enhance spontaneous and auditory-evoked bursts in HVC and RA neurons. Strong burst suppression is mediated mainly via tonically firing HVC-projecting Uva neurons, whereas a fast burst drive is mediated indirectly via Uva neurons projecting to the nucleus interface of the nidopallium. Our results reveal that cerebral sleep-burst epochs and arousal-related burst suppression are both shaped by sophisticated polysynaptic thalamic mechanisms.

Key words: sleep; modulation; arousal; glutamate; lidocaine; GABA; antidromic; orthodromic; acetylcholine; relay; reticular; lemniscus

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Received July 23, 2007; revised Feb. 26, 2008; accepted March 28, 2008.

Correspondence should be addressed to Richard H. R. Hahnloser, Institute of Neuroinformatics, University of Zurich/Swiss Federal Institute of Technology Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland. Email: rich{at}ini.phys.ethz.ch

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