The Journal of Neurophysiology Vol. 85 No. 1 January 2001, pp. 269-279
Copyright ©2001 by the American Physiological Society

Theta Rhythm of Hippocampal CA1 Neuron Activity: Gating by GABAergic Synaptic Depolarization

Laboratory of Adaptive Systems, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, Maryland 20892

Sun, Miao-Kun, Wei-Qin Zhao, Thomas J. Nelson, and Daniel L. Alkon. Theta Rhythm of Hippocampal CA1 Neuron Activity: Gating by GABAergic Synaptic Depolarization. J. Neurophysiol. 85: 269-279, 2001. Information processing and memory consolidation during exploratory behavior require synchronized activity known as hippocampal theta () rhythm. While it is well established that the  activity depends on cholinergic inputs from the medial septum/vertical limb of the diagonal band nucleus (MS/DBv) and  discharges of GABAergic interneurons, and can be induced with cholinergic receptor agonists, it is not clear how the increased excitation of pyramidal cells could occur with increased discharges of GABAergic interneurons during  waves. Here, we show that the characteristic  activity in adult rat hippocampal CA1 pyramidal cells is associated with GABAergic postsynaptic depolarization and a shift of the reversal potential from Cl toward HCO₃ (whose ionic gradient is regulated by carbonic anhydrase). The  activity was abolished by GABA_A receptor antagonists and carbonic anhydrase inhibitors, but largely unaffected by blocking glutamate receptors. Carbonic anhydrase inhibition also impaired spatial learning in a watermaze without affecting other sensory/locomotor behaviors. Thus HCO₃-mediated signaling, as regulated by carbonic anhydrase, through reversed polarity of GABAergic postsynaptic responses is implicated in both  and memory consolidation in rat spatial maze learning. We suggest that this mechanism may be important for the phase forward shift of the place cell discharges for each  cycle during the animal's traversal of the place field for that cell.