In the dorsal hippocampus, A1 adenosine receptor-mediated GirK (G-protein-gated inwardly rectifying potassium) channels conductance is constitutively active contributing to the resting membrane potential of CA1 neurons and preventing from any excitation excess. GirK channel-dependent signaling disruption has been linked to the etiology of many diseases that involve neural excitability alterations, such as Alzheimer’s disease, suggesting an important role of GirK channels for cognitive processes that depend on hippocampal neuronal activity. In the present work, we aimed to explore the role of A1 adenosine receptor-mediated GirK basal activity in the induction and maintenance of synaptic plasticity that supports dorsal hippocampus-dependent cognitive functions. Towards this end, we pharmacologically modulated basal GirK channel conductance in the dorsal hippocampus by using A1 adenosine receptor modulators (agonists: 2’MeCCPA and CPA; antagonist: DPCPX) or by directly manipulating channel activity using ML297, a selective GirK opener, and Tertiapin-Q, a specific GirK blocker, and we examined its involvement in controlling synaptic plasticity processes at different levels of complexity. First, using dorsal hippocampal slices, we studied pharmacological A1 receptor and GirK channel activity modulation effect on the induction and maintenance of long-term synaptic plasticity processes induced in CA1 by Schaffer collateral stimulation. On the other hand, using an in vivo approach, we performed acute intracerebroventricular injections of GirK modulators to study their contribution to CA3-CA1 synapse electrophysiological properties, synaptic plasticity, and non-associative learning and memory capabilities during an open field habituation task. Our data shows that induction and maintenance of long-term synaptic plasticity processes in dorsal hippocampus involves a G-protein dependent mechanism through A1 adenosine receptor-activated GirK, as both A1 receptor and GirK channel activity modulation modified LTP/LTD induction threshold ex vivo (Vehicle (A1 receptor), n = 10, 160 ± 2.4% of baseline, p < 0.001; 2’MeCCPA, n = 5, 95 ± 3.5%, p = 0.806; CPA, n = 5, 109 ± 2.1%, p = 0.216; DPCPX, n = 6, 61 ± 4.1%, p = 0.003; Vehicle (GirK channel), n = 21, 156 ± 1.7% , p < 0.001; ML297, n =12, 73 ± 2.6% of baseline, n = 12, p < 0.001; TQ, n = 13, 95 ± 2.6%, p = 0.007) and in vivo (Vehicle, 184 ± 9% of baseline; n = 9, p = 0.003; ML297, n = 6, 75 ± 8%, p = 0.963; TQ, n = 6, 58 ± 6%, p = 0.508), even switching HFS-induced LTP into LTD. Also, the disruption of such mechanism leads to hippocampal plasticity-dependent learning and memory deficits as shown during the open field habituation task (ML297, n= 8, vs vehicle, n = 10: p = 0.032, TQ, n = 7, vs. vehicle: p = 0.012). These results support the contention that A1 adenosine receptor-mediated GirK basal activity must take place in the hippocampus to sustain its correct functionality and that its dysregulation is detrimental for neural processes underlying cognitive function.