Electrophysiology of the hippocampal and amygdaloid projections to the nucleus accumbens of the rat: convergence, segregation, and interaction of inputs

Abstract

The nucleus accumbens (Nacb) receives inputs from hippocampus and amygdala but it is still unclear how these inputs are functionally organized and may interact. The interplay between these input pathways was examined using electrophysiological tools in the rat, in vivo, under halothane anesthesia. After fornix/fimbria stimulation (Fo/Fi, subicular projection fibers to the Nacb), mono- and polysynaptically driven single units were recorded in the medial shell/core regions of the Nacb and in the ventromedial caudate putamen. Monosynaptically driven neurons by basolateral amygdala (BLA) stimulation were found in the medial shell/core and in the ventrolateral shell/core regions. In the areas of convergence (medial shell/core), paired activation of BLA followed by that of Fo/Fi resulted in an enhancement of the Fo/Fi response, whereas stimulation in the reverse order, Fo/Fi followed by BLA, led to a depression of the BLA response. In addition to these patterns of interactions, the tetanization of the Fo/Fi to Nacb pathway caused a homosynaptic decremental (long-term) potentiation in the Nacb, accompanied by a heterosynaptic (long-term) depression of the nontetanized BLA to Nacb pathway. We postulate that the hippocampal inputs may close a "gate" for the amygdala inputs, whereas the gate is opened for the hippocampus inputs by previous amygdalar activity. These opposite effects on the Nacb neuronal populations should be taken into account when interpreting behavioral phenomena, particularly with respect to the contrasting effects of the amygdala and the hippocampus in locomotion and place learning.

Fig. 1.

Evoked responses recorded in the Nacb. Recording in the medial shell and medial core regions of the Nacb resulted in evoked field potentials with positive peak latencies of ∼10 and 22 msec to Fo/Fi stimulation (A1) and negative peak latencies of ∼16 msec to BLA stimulation (B1), whereas in the ventrolateral shell and core regions, on BLA stimulation, EFPs with longer latencies were recorded (C1). In A2, B2, and C2, single traces (bandpass-filtered) show action potentials that coincide with the positive peaks of the Fo/Fi-induced EFP and the negative peaks of the EFP to BLA stimulation. Peristimulus time histograms of the single unit activity to Fo/Fi and BLA stimulation presented in A3, B3, andC3 were constructed (64 sweeps). Clearly visible is the peak latency at 9 msec to Fo/Fi stimulation (A3) in the medial shell/core and the 15 msec (B3) and 23 msec (C3) peak latency in medial shell/core and ventrolateral shell/core, respectively, to BLA stimulation. The second peak visible in B3 after 21 msec is attributable to the occurrence of an occasional burst of two action potentials.

Fig. 2.

Distribution of single-unit activity within the Nacb to Fo/Fi and BLA stimulation. The transverse sections are modified from the atlas of Paxinos and Watson (1996). Three sections from rostral to caudal Nacb are presented. Top panels, The boundary between shell and core region (short dashes) was based on Jongen-Rêlo et al. (1994) in which calbindin protein staining was used. The circles represent locations where LTP was elicited in the Nacb to Fo/Fi tetanization. Within thecircles, the left symbol relates to the Fo/Fi to Nacb pathway, whereas the right symbol is for the BLA to Nacb pathway. ↑, Potentiation; ↓, depression; −, no effect. + indicates the location where PPF was studied. Bottom panels, Monosynaptically (•) and polysynaptically (○) driven single units to Fo/Fi stimulation and monosynaptically driven single units to BLA stimulation (▴) are presented. Single units presenting mono- and polysynaptic responses to Fo/Fi stimulation are also indicated by filled circles. Single units responding to both Fo/Fi and BLA stimulation are indicated bystar-shaped symbols (filled, monosynaptically driven by Fo/Fi; open, polysynaptically driven by Fo/Fi). Only Fo/Fi-driven units were found in the dorsal shell and the ventromedial caudate putamen (vm CP), whereas only BLA-driven activity was recorded in the ventrolateral part of the Nacb in both shell and core regions. Single units responding to both stimuli were recorded in the medial shell and medial core regions.

Fig. 3.

Distribution of the latencies of Nacb single units driven by Fo/Fi and/or by BLA stimulation. Clearly visible are the two distinct latencies at which Fo/Fi-driven neurons could be found that correspond to the two peaks of the evoked field potential P10 and P25. The BLA-driven units display latencies with peaks at 15 and 19 msec. These single units were all found in the medial shell and medial core regions of the Nacb. Neurons displaying latencies of 20 msec and longer to BLA stimulation were found exclusively in the ventrolateral parts of the Nacb in both shell and core.

Fig. 4.

Examples of paired-pulse interactions of the BLA to Nacb and the Fo/Fi to Nacb pathways. Paired-pulse stimulation of the BLA results in paired-pulse facilitation (A). However, when the conditioning pulse is applied to the Fo/Fi fibers and the test pulse is applied in the BLA, the latter is strongly attenuated (A) compared with a single BLA conditioning pulse with the same intensity. Double-pulse stimulation of the Fo/Fi also results in PPF (B). When the conditioning pulse is applied in the BLA followed by the test pulse in the Fo/Fi, the latter response is enhanced compared with a single Fo/Fi conditioning pulse with the same intensity. The dashed linesrepresent the firing probabilities for the conditioning pulses in these experiments.

Fig. 5.

Long-term interaction between the Fo/Fi and the BLA to Nacb pathways after tetanization of the former. LTP in the Fo/Fi to Nacb pathway is presented after a classic tetanus (50 Hz, 2 sec). The tetanic stimulation was given at t = 0. The LTP shows the characteristic initial increase followed by the decremental phase reaching baseline within 60 min as described previously (Boeijinga et al., 1993; Mulder et al., 1993, 1997). The nontetanized BLA to Nacb pathway is depressed (LTD) significantly for 90 min. Thebars at the bottom of the graph indicate the level of significance for the post-tetanic values compared with the pretetanic controls. Closed bar, Fo/Fi to Nacb;open bar, BLA to Nacb.