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Neural Correlations Increase Between Consecutive Processing Levels in the Auditory System of Locusts

¹Department of Biology, Institute of Behavioural Physiology, Humboldt University Berlin, and ²Center for Molecular Neurobiology Hamburg, University Hamburg, Germany

Submitted 1 August 2006; accepted in final form 28 February 2007

Nervous systems may encode information about sensory stimuli using the temporal relations in spiking patterns between neurons. By conducting simultaneous intracellular recordings on pairs of auditory neurons we measured the strength of correlations between elements of the first three processing levels in the metathoracic auditory network of the locust. We quantified the degree of spike synchronization and rate covariations that occur among auditory neurons during acoustic stimulation. In addition to the acoustic stimulation, current pulses were injected into both neurons to study the connectivity within this network. Our findings support the view that the metathoracic auditory system is a hierarchically organized feedforward network. Strong synaptic connections were observed only between consecutive processing levels, whereas there was no indication for strong connections between elements of the same processing level. Both spike synchronization and rate covariations were increased among neurons on higher processing levels. We further investigated the consequences that correlations may have on the common estimates of neuronal variability. For example, rate covariations caused by strong synaptic coupling between two neurons may lead to an overestimation if the variability is measured trial by trial with respect to only single neurons. For the vast majority of cell pairs tested, however, no strong synaptic coupling could be demonstrated. Thus we could show that in most cases no serious errors are made if one determines variability by following the usual procedure on the basis of single-cell recordings.