Experimental study of the first suckling episode: rat pups ingest fluids through a surrogate nipple

The present study reported a new technique in which pups ingested fluids from a surrogate nipple. Cesarean-delivered pups tested before suckling experience showed oral grasp responses and ingested milk from the surrogate nipple. Pups ingested equal amounts of distilled water and milk and rejected saline. After ingesting milk from the surrogate nipple, pups remained attached to an empty surrogate nipple, while pups exposed to distilled water or saline did not show sustained attachment. Brief experience with milk from an oral cannula or from a surrogate nipple elicited sustained attachment to an empty nipple. Pups ingesting milk from a surrogate nipple showed increased intake of water and saline from the nipple when tested subsequently. The surrogate nipple provides a new technique for experimental study of early suckling behavior. The results suggest that initial experiences with milk may reinforce components of early suckling behavior.     

Sustained attachment to the nipple in the newborn rat depends on experience with the nipple, milk, and the expression of oral grasping.

Newborn rats showed mouthing, licking, and oral grasping when presented with a surrogate nipple. These responses changed after the pup expressed an oral grasp response and experienced milk at the nipple. Newborn pups that ingested milk from the surrogate nipple showed brief oral grasp responses and, when tested 1 hr later, showed sustained attachment to an empty surrogate nipple. Contact with the nipple, oral grasping of the nipple, and experience with milk altered subsequent behavioral responses to the nipple. Classical and instrumental conditioning may play a role in transforming brief oral grasp responses into longer oral grasp responses and sustained attachment to the nipple. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Ontogeny of suckling in rats: Transitions toward adult ingestion.

Studied the suckling behavior of neonatal Sprague-Dawley rats on their own anesthetized mother from the day of birth until after weaning (35 days). Even newborn Ss were capable of nipple attachment without maternal assistance. Before 11–23 days of age, pups deprived of suckling for 22 hrs and nondeprived pups quickly attached to their mother's nipples, sucked, and remained attached to the nipple though no milk delivery occurred. Then behavior underwent at least 3 changes: (a) After 11–23 days of age, latency to attach became considerably elevated in nondeprived pups; (b) a 2nd change in latency occurred at 23–25 days of age, when nondeprived pups no longer even attached to the nipples of anesthetized mothers; and (c) about 14 days of age, deprived pups began to shift from 1 nipple to the next after initial attachment. These developmental changes were seen in other test situations in which pups were placed directly on a nipple and not required to search and when various periods of deprivation were utilized. These transitions were not critically dependent on the onset of visual function or on the pup's experience with food other than mother's milk. Suckling, therefore, in not an unmodified reflex but is an appetitive behavior that undergoes a series of changes during development. These transitions constitute major developmental events in the ontogeny of rat ingestive behavior. (48 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Olfactory aversive conditioning in the newborn (3-hr-old) rat impairs later suckling for water and milk.

An olfactory conditioning paradigm tested whether newborn rats can acquire a conditioned aversion to olfactory events associated with their first postnatal meal 3-5 hr after birth. Exposure to lemon odor (conditioned stimulus [CS]) paired with intraoral infusions of 0.1% quinine (unconditioned stimulus) resulted in explicit conditioning. Responsiveness to a surrogate nipple providing water in the presence of the CS was significantly lower than the 3 control conditions. The conditioning dramatically suppressed responsiveness to a surrogate nipple providing milk, which normally is expressed voraciously in terms of sustained nipple attachment and milk intake. These findings suggest that as early as 3-5 hr after birth newborn rats are capable of aversive conditioning to odors in the context of suckling behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Methysergide-induced nipple attachment depends on suckling experience in juvenile rats.

These studies were designed to investigate the links between pharmacological and behavioral procedures that facilitate suckling in weanling rats by assessing the effects of methysergide on nipple attachment behavior following experiential manipulations known to either promote or attenuate suckling. In the first experiment, methysergide failed to stimulate suckling in 25-day-old rats separated from their dam on Day 20, although it facilitated suckling in rats kept with the dam until either Day 24 or Day 25. In the second experiment, methysergide did not facilitate suckling in 35-day-old rats separated on Day 25, although rats separated on Day 30 or 34 were induced to suckle. In the third experiment, rats were housed with preweanling litters until Day 35 and then separated, housed with 25-day-old litters, or housed with preweanling litters for another 10 days. Rats in a fourth group remained with their dams until Day 35 and were then separated for 10 days. When tested at Day 45, nipple attachment was facilitated by methysergide only in the three groups that had received extended suckling experience. These results demonstrate that serotonergic inhibitory mechanisms modulate nipple attachment only when suckling experience is recent or extensive. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Rapid and robust olfactory conditioning with milk before suckling experience: Promotion of nipple attachment in the newborn rat.

An olfactory conditioning paradigm tested the hypothesis that newborn rats are able to learn about events associated with their first experience with milk as early as 3–5 hr after birth. Exposure to lemon odor (conditioned stimulus, [CS]) paired with intraoral milk infusions (unconditioned stimulus, [US]) resulted in strong conditioning: In the presence of the CS, sustained attachment occurred to an empty nipple as if it provided milk, whereas pups in control conditions showed little attachment. A single CS–US pairing was sufficient for strong conditioning, which was evident with a trace interval as long as 60 s. Conditioning was robust enough to promote attachment to a nipple providing saline, which is aversive to the newborn rat, and comparably strong conditioning occurred with sucrose or saccharin as the US. These findings suggest that olfactory conditioning has the potential to modify suckling behavior. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Self-administration of ethanol and saccharin in newborn rats: Effects on suckling plasticity.

Responsiveness to a surrogate nipple providing water, saccharin, 5% ethanol, or 10% ethanol was tested in newborn rats naive to suckling (3–5 hr old) on Postnatal Day (P) 0 and in older neonates with regular suckling experience on P1 or P2. At all ages, pups demonstrated greater nipple attachment for saccharin or 5% ethanol than for water. Intake of saccharin and 5% ethanol was high in newborns, far exceeding that of water. At P1 and P2, pups exhibited a preference for saccharin, but not for 5% ethanol. Preexposure to a nipple providing ethanol or saccharin (but not a nipple alone or fluids alone) increased subsequent responsiveness toward an empty surrogate nipple (no fluid), both 1 hr and 24 hr after preexposure. Although, during preexposure, pups responded most positively to the nipple providing saccharin, the longest time spent on an empty nipple was observed in pups preexposed to 10% ethanol. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Ontogeny of amphetamine anorexia in rats: A behavioral analysis.

Conducted 4 experiments with 246 Sprague-Dawley rats to ascertain the effects of dextroamphetamine (DAM; 1 or 2 mg/kg) on the behaviors associated with feeding in weanling and preweanling rats. The 1st 2 experiments produced the following results: (a) In 5-day-old Ss, DAM increased speed of approach to an anesthetized mother; (b) at 15 days of age, DAM increased speed of approach to the mother and produced marked weight loss (relative to the weight of controls), slowed or reduced frequency of attachment to the nipple, and decreased time spent nursing; and (c) at 25 days of age, DAM disrupted all aspects of the feeding process except initial approach. Weight gain, time spent in contact with the mother, time spent nursing, and time attached to the nipple were all reduced by the drug. In Exps III and IV, milk was delivered to Ss at 5, 15, and 25 days of age through tongue cannulas, which allowed ingestion without suckling. Under these circumstances, DAM produced clear-cut anorexia in Ss of all 3 ages. It is concluded that in early development, the anorectic effects of DAM are overridden by the strong suckling response that is not disrupted by the drug. (17 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

The role of experience in suckling maintenance in albino rats.

In Exp I nipple-attachment behavior in Sprague-Dawley albino rats was disrupted by raising rat pups in isolation from their mother and siblings on the 3rd–5th day after birth. In Exp II nipple attachment was maintained, however, in isolation-reared pups that received, on Days 3 and 4 postnatally, either 6 or 12 opportunities to search for, locate, and attach to the nipples of an anesthetized mother. Suckling remained severely disrupted on Day 5 in pups whose experiences on Days 3 and 4 were restricted to either nipple search alone or nipple attachment without previous search. Findings focus attention on the role of experience in suckling maintenance and suggest that in rats the suckling system is not fully specified at birth. (35 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Taste aversions to mother's milk: The age-related role of nursing in acquisition and expression of a learned association.

Seven experiments examined the development of taste aversion learning to novel cues contained in mother's milk in 176 laboratory and 377 Sprague-Dawley pups. Ss receiving distinctive milk by experimenter-delivered oral infusions followed by toxicosis formed an aversion to the dam's diet. Robust aversions were learned as early as Day 10 and were retained for at least 11 days. When the same distinctive milk was obtained directly from a foster mother through nursing, only weanling-age Ss formed an aversion. X-ray analysis of nipple location in the mouths of suckling Ss suggested that they receive milk at a similar tongue locus between the ages of 10 and 21 days; flavored milk was then delivered at specific time intervals in controlled quantities through tongue cannulas implanted at loci corresponding to the nipple position. Cannulated preweanling Ss that were attached to a nipple during mild delivery failed to associate the taste cue with illness, whereas both preweanlings off the nipple and weanlings on the nipple acquired aversions to the taste cue in the milk. Results suggest that pups of all ages are incapable of expressing a taste aversion in a nursing situation and that preweanling pups in particular are also deficient in acquiring aversions within a suckling context. The inability of preweanling pups to acquire taste aversions in a nursing situation appears to result from a failure to associate taste cues with illness rather than a failure to detect taste cues obtained from a nipple. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Suckling: Determinants, changes, mechanisms, and lasting impressions.

Four facets of suckling behavior are explored: (a) phylogenetic origins, (b) behavioral and physiological controls of nipple (breast) attachment and milk intake, (c) natural opportunities, through suckling and other classes of filiative behavior, in which to learn about mother, siblings, food, and social status, and (d) mechanisms underlying changes in infant state and affect that might cause long-term emotional and behavioral changes, including ones involved in sexual selection. The article provides, therefore, a means for programmatic investigation of behavioral changes that might be directly or indirectly influenced by early parent contacts. It establishes the temporal and opportunistic limitations that constrain these influences and identifies possible behavioral and physiological mechanisms through which these influences might act. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Fetal experience with milk or an artificial nipple alters appetitive and aversive responses to perioral cutaneous stimuli

Fetal rats exhibit oral grasping of an artificial nipple. The authors examined interactive effects of sensory stimuli normally encountered in the suckling environment on subsequent responses to the nipple. Embryonic Day 20 rat fetuses received an infusion of milk, lemon, or saline through a hollow artificial nipple or an intraoral cannula (producing no nipple stimulation). One minute after sensory pretreatment, behavioral responses of fetuses to an artificial nipple were recorded on videotape for frame-by-frame analysis. Preexposure to the artificial nipple decreased the number of oral grasps and facial wipes directed toward the artificial nipple but increased the duration of grasp responses. Milk uniformly reduced fetal responsiveness to the nipple. Furthermore, the artificial nipple enhanced fetal responses to perioral cutaneous stimulation, whereas milk suppressed perioral responsiveness. These data suggest that the perinatal rat's 1st experience with milk or the nipple can alter subsequent responses to suckling stimuli.     

Stimulus contingencies that permit classical conditioning of opioid activity in the rat fetus.

In a prenatal model of classical conditioning, rat fetuses received presentations of an artificial nipple (conditioned stimulus; CS) paired with milk (unconditioned stimulus). Infusion of milk promotes activity in the kappa opioid system of the fetus, but after 2, 3, or 6 pairings with the artificial nipple, milk evoked both kappa and mu opioid activity. The nipple CS has no effect on opioid activity, but after pairing with milk evoked a mu opioid response. Conditioned mu opioid activity was evident in 60% of subjects tested after I paired conditioning trial. Significantly more fetal subjects (90%) exhibited conditioned opioid activity if preexposed to the nipple twice before conditioning. CS preexposure altered behavior during the conditioning trial, with preexposed fetuses showing more pronounced responses to milk infusion. Exposure to familiar stimuli facilitates classical conditioning of physiological responses, including opioid activity, during the first suckling episode. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Ontogeny of feeding motor patterns in infant rats: An electromyographic analysis of suckling and chewing.

During mammalian ontogeny, there is a transition from suckling to the chewing of food. Is suckling a neuromuscular precursor to chewing, or are suckling and chewing independent systems? Electromyograms (EMGs) were recorded in rat pups of ages 6, 9, 12, 15, 18, and 21 days from the superficial masseter, anterior digastric, sternohyoideus, and genioglossus muscles during suckling and chewing. The EMG patterns of the 3 components of suckling behavior (nipple attachment, rhythmic sucking, and the stretch response) are distinctive from one another and reflect the musculoskeletal biomechanics of suckling. Chewing EMGs are present by 12 days of age and attain the adult pattern by 18–21 days of age. During nipple attachment, pups exhibit a motor pattern that is similar to that of adult chewing, but other aspects of suckling differ from chewing in some EMG features. Comparison of EMGs between behaviors and between ages allowed interpretation of the degree of continuity of muscular activity across the suckling-to-chewing transition. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Separation of opioid from nonopioid mediation of affect in neonatal rats: Nonopioid mechanisms mediate maternal contact influences.

Established a causal distinction in infant rats between opioid- (OP) and non-OP-mediated determinants of behavior. Contact influences were mediated by non-OP pathways, and gustatory influences were OP-mediated. Naltrexone (NTX) did not diminish quieting exerted by contact with an anesthetized dam but reversed the quieting effects of morphine in isolated Ss. Naloxone (NLX) did not affect the latencies with which nondeprived or 8-hr deprived Ss 9, 12, 15, and 18 days old attached to nipples (NPs) of anesthetized dams, nor did NLX cause systematic change in NP attachment in 10- and 18-day old Ss from the NP when milk letdown was induced by oxytocin. NLX did not reduce milk intake in Day-10 Ss that, while suckling, received milk via indwelling cannulae in the anterior portion of the lower jaw or in Ss that obtained milk directly from their awake mother. Milk intake was significantly reduced by NTX in Day-10 Ss that obtained milk by licking it off a saturated substrate. In Day-10 Ss, intake of milk delivered via cannulae was reduced by NLX in Ss that were either isolated, in contact with an anesthetized dam, or attached to her NPs. Behavioral influences of the tactile (and possibly olfactory) qualities of the dam were not mediated by OP systems. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Olfactory, thermal, and tactile controls of suckling in preauditory and previsual rats.

Determined exteroceptive control of nipple attachment in Sprague-Dawley rats and their litters by altering maternal sensory features. Preauditory and previsual pups, 2, 5, 8, and 11 days of age, were permitted to locate and attach to the nipples of their anesthetized mother after she had received one of the following treatments: (a) thermal--peripheral temperature was lowered to either 31 or 28°C; (b) tactile--the mother was shaved; (c) thermotactile--the mother was shaved and her skin temperature was lowered to 31°C; or (d) olfactory--all nipples were cleaned with methylene chloride and alcohol solvents. Only the olfactory treatment severely affected nipple attachment at all ages studied. Washing the nipples virtually eliminated suckling; painting them with a vacuum distillate of the nipple extract or of pup saliva reinstated suckling. The other manipulations either did not interfere with nipple attachment or did so at one age only. (42 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Nipple attachment in rats during the first 24 hours of life.

Investigated nipple attachment in 49 Purdue-Wistar laboratory rat pups during the 1st 24 hrs of life and identified determinants that influenced its expression. In Exp I, nipple attachment was shown to be age dependent: 1-hr-old pups exhibited a low percentage of attachment, and 12- and 24-hr-old pups exhibited high percentages when tested against an anesthetized lactator. Exps II–VI established the time course of nipple attachment as age related. Exps VII–X explored the behavioral mechanism responsible for the increase in attachment from Hr 1 to Hr 12. They showed that nipple experience, independent of milk acquisition, was the responsible factor for the increase. The findings suggest that learning is employed as a behavioral strategy by the newborn, and they reemphasize the value of using species-relevant measures in the assessment of behavioral development. (35 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Opioid control of the fetal stretch response: Implications for the first suckling episode.

On their 1st experience with milk, fetal rats express a stretch response that is similar to the postnatal behavior exhibited by infant rats at the nipple. Fetuses also possess a functional opioid system that is activated by prenatal milk exposure. The opioid receptor antagonist naloxone and the specific kappa antagonist nor-binaltorphimine blocked the stretch response and prevented the increase in rearlimb activity that is typically induced by milk. The mu antagonist β-funaltrexamine blocked the stretch while permitting the expression of rearlimb activity. The kappa agonist U50,488 promoted rearlimb activity in the absence of milk, whereas the mu agonist [{d}-Ala–2,NMe-Phe–4,Gly–5-ol]-enkephalin (DAMGO) exerted little influence on fetal behavior. Fetuses pretreated with U50,488 stretched to nonmilk stimuli (saline or lemon), but fetuses pretreated with DAMGO did not. Opioid activation is part of a chain of events that culminates in the fetal stretch response and may be important in promoting milk ingestion during the newborn's 1st suckling episode. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Classical conditioning of opioid activity in the fetal rat.

Milk promotes activity in the kappa opioid system of the rat fetus that reduces responsiveness to cutaneous stimulation. In this study, fetuses on Gestational Day 20 were presented with an artificial nipple (conditioned stimulus [CS]) paired with an intraoral infusion of milk (unconditioned stimulus [UCS]). One paired presentation of the CS and UCS reduced fetal responsiveness after reexposure to the CS. Selective antagonism of opioid receptors after conditioning indicated that reduced responsiveness was due to mu opioid activity. Mu and kappa opioid activity was evident after 3 paired presentations of CS and UCS and reexposure to milk. Kappa opioid activity during conditioning was necessary for mu involvement after reexposure to the CS or UCS. These experiments, which were conducted with fetal Ss that lacked suckling experience, suggest that neurochemical systems engaged during suckling may change rapidly after the newborn's initial experiences at the nipple. (PsycINFO Database Record (c) 2010 APA, all rights reserved)     

Suckling behavior and intake control in the developing rat pup.

Studied the behavioral development of suckling and intake control in 2 experiments with Charles River CD strain rat pups. Ss were observed at the initiation, during the course, and at the termination of suckling from their anesthetized mothers. Diet was delivered intraorally through a fine tongue cannula which enabled control of timing and volume. The control of diet intake and the behavior at termination of suckling showed correlated changes from 5 to 20 days of age. When deprived of suckling (and food and water) for 8 hr, 5- and 10-day-old Ss consumed large volumes of diet (10% of body weight or greater) and terminated suckling only in the presence of extreme gastrointestinal filling. These Ss were immediately lethargic and slept after intake termination. Five-day-old Ss persisted in reattaching to the nipple when manually stimulated; 10-day-old Ss eventually refused to reattach. In contrast, 20-day-old Ss consumed more moderate volumes of diet (5% of body weight). These Ss also remained awake for a period after feeding and engaged in the exploratory and grooming activities characteristic of adult rats at the termination of feeding. These observations demonstrate major changes in suckling behavior during development. They suggest that intake control processes shift from indirect to direct and become more effective and specifically food intake related in older pups. (20 ref) (PsycINFO Database Record (c) 2010 APA, all rights reserved)