Cortical spreading depression (CSD) is associated with traumatic brain injury (TBI), stroke, migraines, and seizures. Typically, following TBIs and other insults, neuronal excitability in and around the area of the injury is affected, with reported increases in local glutamate signaling. Astrocytic glutamate transporters are critical for precise regulation of the extracellular glutamate availability. However, it remains unclear how impaired astrocytic glutamate transport or an acute TBI affect characteristics of the CSD. We quantified the properties of CSD using whole-cell and extracellular electrophysiological recordings, and voltage-sensitive dye imaging (VSDI) in rat visual cortex in vitro. To model impaired astrocytic glutamate transport, we used astrocytic glutamate transporter blocker (2S, 3S)-3-[3-[4-(trifluoromethyl) benzoylamino] benzyloxy] aspartate (TFB-TBOA). In addition, an acute incision through the superficial cortical layers was used to model the effects of acute traumatic brain injury (TBI) on CSD characteristics. Both manipulations; impaired glutamate cycling and acute cut profoundly affected the physiological properties of cell firing, latency to CSD formation, and its frequency of occurrence. VSD imaging analysis revealed significant changes in spatiotemporal dynamics and propagation of the CSD, suggesting that the cut itself may not initiate CSD depolarizing waves, but rather attract them. Blockade of GLT-1 caused significant reduction in whole-cell sodium currents and changes in CSD wave spatiotemporal characteristics as well, slowing it or even ‘trapping’ its propagation. Our results reveal new information about CSD properties in these pathological conditions and demonstrate an important role of GLT-1 in regulation of CSD.