Major neurotransmitter systems in dorsal hippocampus and basolateral amygdala control social recognition memory

Abstract

Social recognition memory (SRM) is crucial for reproduction, forming social groups, and species survival. Despite its importance, SRM is still relatively little studied. Here we examine the participation of the CA1 region of the dorsal hippocampus (CA1) and the basolateral amygdala (BLA) and that of dopaminergic, noradrenergic, and histaminergic systems in both structures in the consolidation of SRM. Male Wistar rats received intra-CA1 or intra-BLA infusions of different drugs immediately after the sample phase of a social discrimination task and 24-h later were subjected to a 5-min retention test. Animals treated with the protein synthesis inhibitor, anisomycin, into either the CA1 or BLA were unable to recognize the previously exposed juvenile (familiar) during the retention test. When infused into the CA1, the β-adrenoreceptor agonist, isoproterenol, the D1/D5 dopaminergic receptor antagonist, SCH23390, and the H2 histaminergic receptor antagonist, ranitidine, also hindered the recognition of the familiar juvenile 24-h later. The latter drug effects were more intense in the CA1 than in the BLA. When infused into the BLA, the β-adrenoreceptor antagonist, timolol, the D1/D5 dopamine receptor agonist, SKF38393, and the H2 histaminergic receptor agonist, ranitidine, also hindered recognition of the familiar juvenile 24-h later. In all cases, the impairment to recognize the familiar juvenile was abolished by the coinfusion of agonist plus antagonist. Clearly, both the CA1 and BLA, probably in that order, play major roles in the consolidation of SRM, but these roles are different in each structure vis-à-vis the involvement of the β-noradrenergic, D1/D5-dopaminergic, and H2-histaminergic receptors therein.

Keywords: basolateral amygdala; dopamine; hippocampus; norepinephrine; social memory.

Fig. 1.

Effect of Ani given into the CA1 or BLA on the consolidation of SRM. The schematic representation on the top of the figure shows the behavioral protocol used in this and in the following experiments. Animals were subjected to a social discrimination task and, immediately after the sample phase, received intra-CA1 (A; 1 µL per side) or intra-BLA (B; 0.5 µL per side) infusions of vehicle (Veh) or Ani (100 µg per side). Twenty-four hours later, animals were subjected to a 5-min retention test in the presence of the familiar juvenile (F) and a novel one (N). Dots indicate the theoretical mean of 50%. Data are expressed as mean ± SEM (n = 8–10 animals per group) and presented as percentage of total exploration time. *P < 0.05 and ***P < 0.001 Veh-N vs. Ani-N, Bonferroni’s Multiple Comparison test after one-way ANOVA.

Fig. 2.

Effect of β-adrenoreceptor antagonist and agonist infused into the CA1 or into the BLA on the consolidation of social recognition memory. Animals were subjected to a social discrimination task and immediately after the sample phase received intra-CA1 (A; 1 µL per side) or intra-BLA (B; 0.5 µL per side) infusions of vehicle (Veh), Tim (1.0 µg per side), or Iso (10.0 µg per side) or coinfusion of Timolol plus Isoproterenol (Tim+Iso). Twenty-four hours later, animals were subjected to a 5-min retention test in the presence of the familiar juvenile (F) and a novel one (N). Dots indicate the theoretical mean of 50%. Data are expressed as mean ± SEM (n = 8–12 animals per group) and presented as percentage of total exploration time. *P < 0.05 Veh-N vs. Iso-N (CA1), Veh-N vs. Tim-N (BLA), Bonferroni’s Multiple Comparison test after one-way ANOVA. In this and in Fig. 3, note that the drug effects were more intense in the CA1 than in BLA, probably indicating a larger importance of the former in modulation of this behavior both by noradrenergic receptors (this figure) and dopaminergic receptors (Fig. 3).

Fig. 3.

Effect of D1/D5 dopamine receptors antagonist and agonist infused into the CA1 or into the BLA on the consolidation of social recognition memory. Animals were subjected to a social discrimination task and immediately after the sample phase received intra-CA1 (A; 1 µL per side) or intra-BLA (B; 0.5 µL per side) infusions of vehicle (Veh), SCH23390 (SCH; 1.50 µg per side) or SKF38393 (SKF; 12.5 µg per side), or coinfusion of SCH23390 plus SKF38393 (SCH+SKF). Twenty-four hours later, animals were subjected to a 5-min retention test in the presence of the familiar juvenile (F) and a novel one (N). Dots indicate the theoretical mean of 50%. Data are expressed as mean ± SEM (n = 9–12 animals per group) and presented as percentage of total exploration time. *P < 0.05 Veh-N vs. SKF-N (BLA); **P < 0.01 Veh-N vs. SCH-N, Bonferroni’s Multiple Comparison test after one-way ANOVA.

Fig. 4.

Effect of H2 histamine receptors antagonist and agonist infused into the CA1 or into the BLA on the consolidation of social recognition memory. Animals were subjected to a social discrimination task and immediately after the sample phase received intra-CA1 (A; 1 µL per side) or intra-BLA (B; 0.5 µL per side) infusions of vehicle (Veh), Rani (17.5 µg per side), or Dima (2.3 µg per side), or coinfusion of Rani plus Dima (Rani+Dima). Twenty-four hours later, animals were subjected to a 5-min retention test in the presence of the familiar juvenile (F) and a novel one (N). Dots indicate the theoretical mean of 50%. Data are expressed as mean ± SEM (n = 8–12 animals per group) and presented as percentage of total exploration time. *P < 0.05 Veh-N vs. Rani-N, Bonferroni’s Multiple Comparison test after one-way ANOVA.