Amphetamine is used in the therapy of mental disorders and for recreational purposes. However, repeated exposures lead to amphetamine sensitization (AS), which is associated with hyperdopaminergia, cognitive dysfunctions, and aberrant behavior. Notably, mounting evidence indicates that activation of group II metabotropic glutamate receptors (mGluR2 and mGluR3) reverses neuroplasticity associated with AS and prevents both, anxiety and psychosis, in rodent models.We employed a system-oriented approach, murine model of AS, and selective pharmacological tools to explore the specific contribution of mGluR2 and mGluR3 in counteracting the impact of amphetamine on the motive system. In-vivo electrophysiological recordings were conducted under anaesthesia to determine the activity states of ventral tegmental area (VTA) dopamine (DA) neurons. Consistent with previous studies, repeated exposure to amphetamine (2mg/kg; daily, for five days) followed by drug withdrawal, disrupted tonic DA firing (i.e. population activity). Thus, following short withdrawal, hypodopaminergic states were assessed in VTA, which resulted secondary to hyperactivity at the amygdala-nucleus accumbens (NAc) synapse. Activation of mGluR2 by the positive allosteric modulator LY487379 reversed both, low DA neuron firing and negative affective states, by exploiting the NAc indirect pathway. On the other end, prolonged withdrawal elicited aberrant firing in both, VTA and ventral hippocampus (vHPC). Notably, either inactivation of vHPC by TTX or in-situ deposits of the selective mGluR3 agonist LY2794193 normalized network dynamics within the vHPC-VTA circuits. Moreover, LY2794193 also reversed hyperlocomotor activity, which is associated with AS.Thus, rewiring glutamatergic transmission within vHPC-VTA circuit represents a successful strategy in counteracting AS and resolving psychotic symptoms.