Serotonergic control of ingestive and post-ingestive behaviors in pigeons (Columba livia): The role of 5-HT1A receptor-mediated central mechanisms

Abstract

Central injections of serotonin (5-HT) produce hyperdipsic and hypnogenic behavioral effects that are correlated to decreased Fos-immunorreactivity of 5-HT neurons in free-feeding pigeons. We herein (1) probed the role of 5-HT1A receptors on the 5-HT- or 8-OH-DPAT-evoked postprandial behaviors and (2) described the sleep–waking states (waking, W; drowsiness, D; slow-wave sleep, SWS; rapid-eye movement sleep, REMS) and sleep architecture of free-feeding pigeons after these treatments. Latency, frequency and duration of feeding, drinking, preening, exploratory and sleep-like behaviors (SLB) were examined after intracerebroventricular (ICV) injections of 5-HT (0, 50 or 150nmol) or 8-OH-DPAT (DPAT, 0 or 30nmol) in pigeons pretreated with the 5-HT1A antagonist WAY100635 (WAY, 0, 0.1, 0.3 or 1nmol). Additionally, the acute (1h) waking-sleep-related electrographic activity in the hippocampus (HP) was examined after ICV injections of 5-HT (150 or 300nmol) or DPAT (30 or 60nmol) in pigeons pretreated with WAY (0 or 1nmol). 5-HT and DPAT acutely increased drinking and then sleep: all doses of WAY attenuated the 5-HT (50nmol) -induced dipsogenic effect, but left unchanged the effects of the 150nmol 5-HT dose. The WAY 0.1nmol dose blocked the SLB induced by the 5-HT 50nmol dose. Given before the vehicle (VEH) injections, WAY does not affect water or food intake, but increased the SLB duration at all doses. DPAT injections increased feeding, drinking and SLB. All the WAY doses attenuated the DPAT-induced drinking and feeding responses, and the WAY 0.1 and 0.3nmol doses reduced DPAT-induced SLB. DPAT or 5-HT injections decreased the duration of electrographically-determined waking, increased the durations of D and induced the emergence of SWS and REMS states indistinguishable from the hippocampal EEG associated with spontaneous sleep, as judged from visual and spectral analysis. WAY (1nmol) increased SWS and D, and potentiated the 5-HT- and DPAT-induced SWS. These data suggest that 5-HT-induced drinking depends on the activation of presynaptic 5-HT1A receptors, while 5-HT1A autoreceptor activation contributes to the 5-HT-induced sleep. 5-HT-induced drinking and sleep behaviors may thus be provoked by a 5-HT1A-evoked, rebound-like reduction in central 5-HTergic activity. These data also indicate that an ongoing, tonic and inhibitory influence of central 5-HT circuits may participate in the control of feeding, drinking and rest behaviors in pigeons during the wake, nibbling diurnal state. These mechanisms appear to be comparable to those found in mammals, suggesting that they may represent a conserved, plesiomorphic functional trait of the amniotes brain.