Michael E. Rashotte

Second-order conditioning of the pigeon’s keypeck

Pigeons learned to peck a keylight (S2) when it was paired with a stimulus (S1) that already evoked keypecking. Control procedures showed that S2 acquired control over responding because it was paired with S1 and because S1 had a conditioning history, thereby supporting the claim that S2 was a second-order conditioned stimulus. Second-order conditioning occurred as rapidly when S1 was a keylight as when it was a tone. Test procedures showed that after second-order conditioning, responding to S2 was markedly debilitated by the extinction of responding to S1, indicating that the ability of S2 to evoke a response importantly depends upon the continued ability of S1 to do so. Our demonstration that directed motor action in the pigeon is susceptible to second-order conditioning suggests a new interpretation of conditioned reinforcement in instrumental learning. Our demonstration that the effectiveness of S2 depends upon the continued effectiveness of S1 indicates that S-S associations are formed in this version of the second-order conditioning experiment.

Associative influence on the foraging behavior of pigeons (Columba livia).

In a laboratory simulation of foraging conditions, pigeons maintained ad lib weight by treadle pressing for lengthy periods of access to grain in a 24-hr live-in environment. Localized visual signals produced by treadle pressing evoked approach and pecking behavior if they signaled impending food presentation (Pavlovian first-order conditioning) or the presentation of an established signal for food (Pavlovian second-order conditioning). These findings imply a role for associative mechanisms in the control of foraging.

Daily cycles in body temperature, metabolic rate, and substrate utilization in pigeons: influence of amount and timing of food consumption

Pigeons lived in individual chambers where instantaneous metabolic rate (MR; indirect calorimetry), body temperature (Tb), and substrate utilization (RQ) were measured 24 times each hour throughout the 12h:12h light:dark cycle. The amount of food consumed influenced the amplitude of the MR and Tb cycles, primarily by affecting the dark-phase segment of the cycle: when food was consumed ad lib, low-amplitude daily cycles in MR and Tb occurred in which levels in the dark phase were lower than in the light; during reduced food intake in restricted feeding or in fasting, high-amplitude cycles occurred primarily because nocturnal hypometabolism and hypothermia developed; in restricted feeding, the level of MR and Tb during the dark-phase segment of the cycle was directly related to short-term variation in amount consumed. The timing of food consumption primarily affected the light-phase segment of the MR and Tb cycles: when feeding was restricted to a time late in the light phase, these measures became depressed early in the light phase, and then greatly elevated near the scheduled time of feeding. This distinctive light-phase pattern developed quickly after the restricted feeding schedule began and may reflect the influence of a circadian food-entrainable oscillator. RQ indicated carbohydrate utilization for most of the 24-h cycle during ad lib feeding and in restricted feeding. However, approximately 2 h before the first feeding bout of the day, the RQ cycle indicated a sizable shift towards lipid utilization, which terminated after the bout was completed. There was a smaller, more transient, decrease in RQ near the time of the light-dark transition, which may imply cessation of digestive activity in preparation for the nocturnal decrease in Tb. During fasting, RQ indicated lipid utilization throughout the entire cycle. Whole-day energy expenditure by pigeons in these laboratory circumstances was shown to be closely related to the changes in within-day cycles associated with variations in the amount and timing of food intake.

Vigilance states and body temperature during the circadian cycle in fed and fasted pigeons (Columba livia)

Fasting induces nocturnal hypothermia in pigeons. Slow-wave sleep (SWS) and paradoxical sleep (PS) are associated with reduced heat production in pigeons. The possibility that fasting-induced nocturnal hypothermia is related to increased SWS and PS was examined by comparing body temperature (Tb) and vigilance states when pigeons were fed and fasted. The results showed that when Tb is decreasing near the beginning of the dark phase, the percentage of total recording time (%TRT) spent in SWS and PS was elevated in fasting due to increased frequency of episodes and increased duration of PS episodes. When Tb was low during the middle segment of the dark phase, SWS was elevated in fasting due to increased episode duration. However, fasting did not alter PS, which increased in %TRT across the segment due to increased episode frequency. When Tb was rising during the final hours of dark, SWS remained elevated in fasting and %TRT in SWS and PS was relatively high. SWS and PS may promote the fasting pigeons entry into, and maintenance of, nocturnal hypothermia.Fasting induces nocturnal hypothermia in pigeons. Slow-wave sleep (SWS) and paradoxical sleep (PS) are associated with reduced heat production in pigeons. The possibility that fasting-induced nocturnal hypothermia is related to increased SWS and PS was examined by comparing body temperature (Tb) and vigilance states when pigeons were fed and fasted. The results showed that when Tb is decreasing near the beginning of the dark phase, the percentage of total recording time (%TRT) spent in SWS and PS was elevated in fasting due to increased frequency of episodes and increased duration of PS episodes. When Tb was low during the middle segment of the dark phase, SWS was elevated in fasting due to increased episode duration. However, fasting did not alter PS, which increased in %TRT across the segment due to increased episode frequency. When Tb was rising during the final hours of dark, SWS remained elevated in fasting and %TRT in SWS and PS was relatively high. SWS and PS may promote the fasting pigeons entry into, and maintenance of, nocturnal hypothermia.

Central Leptin Infusion Attenuates the Cardiovascular and Metabolic Effects of Fasting in Rats

The role of reduced leptin signaling in the regulation of cardiovascular responses to negative energy balance is not known. We tested the hypothesis that central infusion of leptin would attenuate the cardiovascular and metabolic responses to fasting. Male Sprague-Dawley rats, instrumented with telemetry devices and intracerebroventricular cannulas, were housed in metabolic chambers for continuous (24 hours) measurement of dark-phase (active) and light-phase (inactive) mean arterial pressure, heart rate, oxygen consumption, and respiratory quotient. Rats received central infusions of either saline (0.5 &mgr;L/h) or leptin (42 ng/h) for 6 days through osmotic pumps and were either fed ad libitum or were fasted for 48 hours followed by refeeding for 4 days. In ad lib animals, continuous intracerebroventricular leptin infusion significantly reduced caloric intake, body weight, and respiratory quotient compared with saline controls while having no effect on mean arterial pressure or heart rate. Fasting reduced mean arterial pressure, heart rate, oxygen consumption, and respiratory quotient in rats receiving saline infusions. Fasting-induced reductions in mean arterial pressure were specific to the active phase and were not attenuated by central leptin infusion. In contrast, intracerebroventricular leptin, at a dose that had no cardiovascular effects in ad lib control animals, completely prevented fasting-induced decreases in light-phase heart rate and oxygen consumption and blunted fasting-induced reductions in dark-phase heart rate and oxygen consumption. The results are consistent with the hypothesis that reductions in central leptin signaling contribute to the integrated cardiovascular and metabolic responses to acute caloric deprivation.

Energetic responses of pigeons during food deprivation and restricted feeding

Pigeons ate food ad lib, then fasted for several days, and finally ate a controlled amount of food once a day for several months to maintain body weight at 80% of the ad lib value. Whole-body dry heat loss (HL) and core body temperature (Tb) were measured continuously for each pigeon. Thermal conductance (C) was calculated from HL and Tb. Relative to ad lib feeding, 24-h HL was reduced by approximately 50% during fasting and controlled feeding. The majority of energy savings was achieved by lowering C, which appeared to maintain a saturated low value throughout most of the light and dark phases. Therefore, the pigeons characteristic high Tb in the daily light phase during fasting and food restriction does not necessarily imply high energy expenditure. In the dark phase, the fasting pigeons characteristically low Tb enhances energy savings already being achieved through lowered C. The daily cycle in Tb, and to a lesser extent in HL and C, was strongly altered by occasional probe variations in the amount of food given at the single daily feeding and by a shift in the time of the daily feeding.

Shivering thermogenesis in the pigeon: the effects of activity, diurnal factors, and feeding state

Shivering (electromyographic activity of the pectoral muscle), oxygen consumption, and body temperature were measured from undisturbed pigeons for periods of several weeks, and segments from the midparts of each phase of the light-dark cycle were compared at various ambient temperatures and feeding regimes. Behavior was recorded with a video camera. None of the observed types of behavior (e.g., walking, preening, feeding, drinking, pecking, defecation) induced spurious electrical activity in the pectoral muscle. On the other hand, none of these behaviors directly inhibited ongoing shivering. There was no difference in the mean level of shivering between the light (L) and dark (D) phases of the day in any of the conditions, although body temperature was 2°C higher during L. Measurements of integrated electromyogram (EMG) with high temporal resolution (28 samples/s) showed that, at 1°C, shivering in the pectoral muscle was present for more than 98% of the time. Plots of oxygen consumption against root mean square EMG were obtained in each condition by a filtering procedure that excludes data points in which oxygen consumption is affected by motor activity. These plots showed that the increase in heat production induced by a unit increase in pectoral EMG was lower in D than in L and that it was further lowered by fasting. The amplitude spectra of raw EMG signals were similar in all conditions. Spectra of demodulated (rectified, low-pass filtered) EMG showed a distinct rhythmicity around 8 Hz at 21°C that was further enhanced by fasting but absent at 1°C. This suggests that the degree of synchronization and pattern of recruitment of motor units are specific for various temperatures and feeding regimes, and may partly explain the variable relation between heat production and muscle electrical activity. The results emphasize the advantages of long-term measurements for understanding the control of thermogenesis in birds.

Shivering and digestion-related thermogenesis in pigeons during dark phase

The pigeons main source of regulated heat production, shivering, is especially likely to be used for thermoregulation during the dark phase of the day when there is little heat from locomotor activity. However, food stored in the pigeons crop is digested during the night, and digestion-related thermogenesis (DRT) will provide heat that should decrease the need for shivering to maintain body temperature (Tb). We investigated the conditions under which DRT alters the occurrence of nocturnal shivering thermogenesis in pigeons. In fasting experiments, in which DRT was minimal, variations in pectoral shivering were closely related to the kinetics of nocturnal Tb when the ambient temperature (Ta) was moderate (21°C). In that case, shivering was low while Tb fell at the beginning of the night, moderate during the nocturnal plateau in Tb, and strong during the prelight increase in Tb. Similar kinetics of nocturnal Tb occurred when Ta = 28°C, but shivering was negligible throughout the dark phase. In restricted feeding experiments, nocturnal DRT was varied by providing different amounts of food late in the light phase. When Ta = 21°C, 11°C, and 1°C, nocturnal Tb and O2 consumption were directly related to the amount of food ingested. However, nocturnal shivering tended to decrease as the food load increased and was significantly reduced at the higher loads. Because nocturnal shivering did not become more efficient in producing heat as the size of the food load increased, we conclude that nocturnal DRT decreased the need for shivering thermogenesis.The pigeons main source of regulated heat production, shivering, is especially likely to be used for thermoregulation during the dark phase of the day when there is little heat from locomotor activity. However, food stored in the pigeons crop is digested during the night, and digestion-related thermogenesis (DRT) will provide heat that should decrease the need for shivering to maintain body temperature (Tb). We investigated the conditions under which DRT alters the occurrence of nocturnal shivering thermogenesis in pigeons. In fasting experiments, in which DRT was minimal, variations in pectoral shivering were closely related to the kinetics of nocturnal Tb when the ambient temperature (Ta) was moderate (21 degrees C). In that case, shivering was low while Tb fell at the beginning of the night, moderate during the nocturnal plateau in Tb, and strong during the prelight increase in Tb. Similar kinetics of nocturnal Tb occurred when Ta = 28 degrees C, but shivering was negligible throughout the dark phase. In restricted feeding experiments, nocturnal DRT was varied by providing different amounts of food late in the light phase. When Ta = 21 degrees C, 11 degrees C, and 1 degrees C, nocturnal Tb and O2 consumption were directly related to the amount of food ingested. However, nocturnal shivering tended to decrease as the food load increased and was significantly reduced at the higher loads. Because nocturnal shivering did not become more efficient in producing heat as the size of the food load increased, we conclude that nocturnal DRT decreased the need for shivering thermogenesis.

Evidence for a separate food-entrainable circadian oscillator in the pigeon

In Experiment 1, four pigeons lived in a metabolic chamber on a 12h:12h LD cycle where they maintained a reduced body weight by consuming a daily ration of food presented at the eighth hour of the photophase. Body temperature (Tb) and oxygen consumption (Vo2) increased prior to the daily feeding. The possibility that a food-entrainable oscillator timed these anticipatory responses was tested by four manipulations, conducted in successive phases, each of which involved eliminating the regularly scheduled food presentation, which is the putative entraining stimulus for such an oscillator, while the 12h:12h LD cycle remained in effect. The manipulations, and their outcomes, were: when fasting was imposed for 3 days, the anticipatory responses continued to occur; when ad lib feeding was allowed for 11 days, the anticipatory responses were mostly eliminated; when fasting was reimposed for 5 days, there was evidence that the anticipatory responses reoccurred; and, when the time of the daily feeding was phase-shifted earlier in the photophase for 8 days, anticipatory responses persisted at the original feeding time and simultaneously developed at the new feeding time. In the first phase of Experiment 2, key pecking by two pigeons produced food only during hours 9-11 of the daily photophase (12h:12h LD). In this condition, Tb increased and key pecking occurred in anticipation of the daily period of food availability. Evidence for a food-entrained oscillator was sought in a second phase when constant dim light (LL) was imposed without changing the hours of food availability.(ABSTRACT TRUNCATED AT 250 WORDS)

Coupling between light- and food-entrainable circadian oscillators in pigeons

Two experiments were conducted with a restricted feeding schedule to determine whether pigeons have a separate food-entrainable oscillator (FEO) and to assess the coupling strength between the FEO and the light-entrainable oscillator (LEO). In the baseline condition, the body temperature (Tb) and O2 consumption of two pigeons increased prior to light onset (LD 12:12 cycle) and food presentation (at the ninth hour of the light phase). In one experiment, when the LD cycle was phase delayed or advanced by 4 h while feeding time remained unchanged, the Tb and O2 rises prior to light-onset showed the expected delaying or advancing transients, but the rises prior to feeding also delayed or advanced for several days before returning to their proper phase position. In the second experiment, food was presented at 23.5-h intervals for 10 days while the LD cycle continued with a 24-h period. Entrainment to the LD cycle was unaffected, and Tb and O2 consumption continued to rise prior to the changing feeding time, but with a reduced lead time. When the feeding time was subsequently delayed by 5 h, Tb and O2 consumption with regard to the LD cycle were unaffected, but delaying transients occurred until both measures reentrained to the new feeding time. The results provide support for the existence of a separate FEO in pigeons and indicate asymmetrical coupling between the LEO and FEO, with the former having a stronger effect on the latter.