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The Journal of Neuroscience, October 14, 2009, 29(41):12886-12895; doi:10.1523/JNEUROSCI.3491-09.2009

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Behavioral/Systems/Cognitive
Convergence of Cranial Visceral Afferents within the Solitary Tract Nucleus

Stuart J. McDougall, James H. Peters, and Michael C. Andresen

Department of Physiology and Pharmacology, Oregon Health & Science University, Portland, Oregon 97239-3098

Correspondence should be addressed to Dr. Stuart J. McDougall, Department of Physiology and Pharmacology, L334, Oregon Health & Science University, 3181 Southwest Sam Jackson Park Road, Portland, OR 97239-3098. Email: stuart.mcdougall{at}gmail.com

Primary afferent axons within the solitary tract (ST) relay homeostatic information via glutamatergic synapses directly to second-order neurons within the nucleus of the solitary tract (NTS). These primary afferents arise from multiple organ systems and relay multiple sensory modalities. How this compact network organizes the flow of primary afferent information will shape central homeostatic control. To assess afferent convergence and divergence, we recorded ST-evoked synaptic responses in pairs of medial NTS neurons in horizontal brainstem slices. ST shocks activated EPSCs along monosynaptic or polysynaptic pathways. Gradations in shock intensity discriminated multiple inputs and stimulus recruitment profiles indicated that each EPSC was unitary. In 24 pairs, 75% were second-order neurons with 64% receiving one direct ST input with the remainder receiving additional convergent ST afferent inputs (22% two; 14% three monosynaptic ST-EPSCs). Some (34%) second-order neurons received polysynaptic EPSCs. Neurons receiving only higher-order inputs were uncommon (13%). Most ST-EPSCs were completely independent, but 4 EPSCs of a total of 81 had equal thresholds, highly correlated latencies, and synchronized synaptic failures consistent with divergence from a single source ST axon or from a common interneuron producing a pair of polysynaptic EPSCs. We conclude that ST afferent inputs are remarkably independent with little evidence of substantial shared information. Individual cells receive highly focused information from the viscera. Thus, afferent excitation of second-order NTS neurons is generally dominated by single visceral afferents and therefore focused on a single afferent modality and/or organ region.

Received July 17, 2009; revised Aug. 21, 2009; accepted Aug. 29, 2009.

Correspondence should be addressed to Dr. Stuart J. McDougall, Department of Physiology and Pharmacology, L334, Oregon Health & Science University, 3181 Southwest Sam Jackson Park Road, Portland, OR 97239-3098. Email: stuart.mcdougall{at}gmail.com






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