Neuronal pair and triplet interactions in the auditory midbrain of the leopard frog

Abstract

1. With the use of two independent microelectrodes and multiunit spike separation, 26 neural pairs, 17 triplets, and 8 quadruplets were recorded in the auditory midbrain of the leopard frog, resulting in a total of 125 neural pairs. 2. Functional interrelationships between neurons were studied by analyzing 638 cross-coincidence histograms as functions of stimulus type, stimulus level, and estimated neuron distance. Significance criteria for correlograms were established on the basis of the distribution of extreme values in a large number of correlograms for nonsimultaneously recorded pairs. 3. Simultaneous recordings from three neurons, that all showed significant neural pair correlations were analyzed with the use of the joint occurrence diagram, which displays the joint coincidences for the firings of two units (a and b) with the firings of the trigger unit (c). 4. It was found that 97.5% of the pairs showed a significant stimulus-induced correlation; neighboring neurons exhibited a stronger stimulus correlation (synchrony) than more distant neurons. 5. Positive neural interaction strength (75% to shared excitatory input) was independent of neuron distance (taking into account that the estimated electrode distance in the present investigation was never greater than 300 microns) and occurred in 25% of the pairs investigated. About 25% of the positive neural correlations could be attributed to unidirectional excitation, the majority of which was found for single-electrode pairs. Negative neural correlation occurred in 8% of the pairs and, with one exception, was found only for neurons recorded on the same electrode. 6. Evidence for the presence of feed-forward and/or feedback inhibition was found. 7. There was a strong stimulus-type influence on stimulus correlation and on positive neural correlation, whereas stimulus intensity affected the stimulus correlation but not the neural correlation. 8. From the incidence of triplet correlations, it was concluded that the divergence of afferents onto midbrain neurons was limited; it was unlikely that more than three neurons were contacted by one afferent. In contrast, convergence of afferents on torus semicircularis cells was widespread; 40-50% of the midbrain neurons were bimodally tuned and received input originating from the two auditory papillae. Convergence of fibers from the same papilla was also extensive. 9. Fast modulation of functional neural connectivity through the activity of other neurons was found, although this was probably not the result of actual changes in synaptic strength but of synchronized changes in firing rate.