CB1 cannabinoid receptors (CB1Rs) are widely expressed throughout the brain, particularly in areas involved in learning and memory, such as the hippocampus. In the CA1 area, they are mainly present at the presynaptic terminals of both GABAergic and glutamatergic neurons. The antagonist/inverse agonist AM251 is a useful pharmacological tool due to its high selectivity and ability to tap into the endocannabinoid system (ECS). When infused into the brain, it interferes with the natural functioning of the local pool of endocannabinoids present at each memory phase, and by enhancing or suppressing the natural course of events, it unveils its “normal” function in each situation. Anandamide (AEA) was also studied, but results were less consistent. A large set of experiments show that different memory phases are modulated by the ECS in opposite, complementary ways: AM251 was amnestic (and AEA, facilitatory) when infused into CA1, both after training (consolidation) or after a long reactivation session (extinction), suggesting that ECS modulates positively these two phases. On the other hand, AM251 facilitated (and AEA frequently disrupted) memory when administered before test (retrieval) or after a short reactivation session (reconsolidation), suggesting a negative modulatory role. Thus, symmetrically opposed actions seem to be the rule for the ECS role, at least in the CA1 area, suggesting it modulates both plasticity events and the selection or “switching” between, for instance, extinction and reconsolidation. Findings were interpreted according to a simplified CA1 Local Circuit Model and the most probable position / level of expression of presynaptic cannabinoid CB1 receptors. The ECS ubiquity in mammal brains is consistent with its multifunctional, fine-tuning modulatory role behind complex cognitive mechanisms, such as the directioning of mnemonic outcome.