Neurons in the rodent anteroventral periventricular nucleus (AVPV) play a key role in integrating circadian and gonadal steroid hormone information in the control of fertility. In particular, estradiol-sensitive kisspeptin neurons located in the AVPV, and adjacent structures [together termed the rostral periventricular area of the third ventricle (RP3V)], are critical for puberty onset and the preovulatory LH surge. The present study aimed to establish the morphological and electrical firing characteristics of RP3V neurons, including kisspeptin neurons, in the adult female mouse. Cell-attached electrical recordings, followed by juxtacellular dye filling, of 129 RP3V neurons in the acute brain slice preparation revealed these cells to exhibit multipolar (53%), bipolar (43%), or unipolar (4%) dendritic morphologies along with silent (16%), irregular (41%), bursting (25%), or tonic (34%) firing patterns. Postrecording immunocytochemistry identified 17 of 100 filled RP3V cells as being kisspeptin neurons, all of which exhibited complex multipolar dendritic trees and significantly (P < 0.05) higher bursting or high tonic firing rates compared with nonkisspeptin neurons. The firing pattern of RP3V neurons fluctuated across the estrous cycle with a significant (P < 0.05) switch from irregular to tonic firing patterns found on proestrus. A similar nonsignificant trend was found for kisspeptin neurons. All RP3V neurons responded to gamma-aminobutyric acid and glutamate, about 10% to RFamide-related peptide-3, about 5% to vasopressin, 0% to vasoactive intestinal peptide, and 0% to kisspeptin. These studies provide a morphological and electrical description of AVPV/RP3V neurons and demonstrate their cycle-dependent firing patterns along with an unexpected lack of acute response to the circadian neuropeptides.