Position and behavioral modulation of synchronization of hippocampal and accumbens neuronal discharges in freely moving rats

To understand how hippocampal signals are processed by downstream neurons, we analyzed the relative timing between neuronal discharges in simultaneous recordings in the hippocampus and nucleus accumbens of rats performing in a plus maze. In all, 154 pairs of cells (composed of 65 hippocampal and 56 accumbens neurons) were examined during the 1 s period prior to reward deli very. Cross-correlation analyses over a +/-300-ms window with 10-ms bins re vealed that 108 pairs had at least one significant histogram bin (P < 0.01) . The most frequently occurring peaks of hippocampal firing prior to accumb ens discharges appeared at latencies from -30-0 ms, corresponding to publis hed values of the latency of the hippocampal pathway to the nucleus accumbe ns. Other peaks appeared most often at latencies multiples of about 110 ms prior to and after this, corresponding to theta rhythmicity. Since firing s ynchronization can result from several types of connectivity patterns (such as common inputs), a group of 18 hippocampus-accumbens pairs was selected as those most likely to have monosynaptic connections. The criterion was th e presence of at least one highly significant peak (P < 0.001) at latencies corresponding to field potentials evoked in the accumbens by hippocampal s timulation. A significant peak occurred on all four maze arms for only one of these cell pairs, indicating positional modulation for the others. In ad dition, behavior dependence of the synchrony between these nucleus accumben s and hippocampus neurons was examined by studying data in relation to thre e different synchronization points: reward box arrival, box departure, and arrival at the center of the maze. This indicates that the functional conne ctivity between hippocampal and accumbens neurons was stronger when the rat was near reward areas. Ten of the hippocampal neurons in these 18 cell pai rs showed 9-Hz (theta) rhythmic activity in autocorrelation analyses. Of th ese 10 cells, cross-correlograms from eight hippocampal-accumbens pairs als o showed theta rhythmicity. Overall, these results indicate that the synchr ony between hippocampus and nucleus accumbens neurons is modulated by spati al position and behavior, and theta rhythm may play an important role for t his synchronization. Hippocampus 2000;10:717-728. (C) 2000 Wiley-Liss, Inc.