William P. Smotherman

Odor aversion learning by the rat fetus

Rat fetuses were exposed to an odor stimulus on day 20 of gestation via amniotic injection and then injected with LiCl. In a CER paradigm, 10 day old pups were trained to approach an anesthetized dam in a runway for suckling reinforcement. When running speeds had stabilized the odor stimulus experienced in-utero was introduced into the test chamber. This odor took on aversive properties as a function of its pairing with LiCl, as evidenced by a decrease in running speed on CER trials and increases in the number of trials that were terminated because pups failed to traverse the runway. These data indicate that the fetal rat is capable of odor aversion learning.

In utero taste/odor aversion conditioning in the rat

Rat fetuses exposed to a taste-odor stimulus and an aversive stimulus in utero showed an aversion to the taste/odor stimulus when tested 16 days postnatally. Fetuses which received various control treatments in utero did not show an aversion. These data show that rat fetuses at 20 days of gestation are capable of associative learning which can be demonstrated more than two weeks postnatally.

The Rat Fetus in Its Environment: Behavioral Adjustments to Novel, Familiar, Aversive, and Conditioned Stimuli Presented In Utero

With the pregnant rat under ether anesthesia, rat fetuses were exposed on Day 17 of gestation to a taste/odor stimulus (mint) injected into the amniotic fluid and/or lithium chloride injected into the peritoneum. Behavior of injected fetuses was directly observed on Day 19 of gestation following chemomyelotomy and laparotomy of the female and immersion of the uterus into a warm saline bath. With these procedures, a series of four experiments was conducted to assess the behavioral effects of (a) the mint taste/odor alone, (b) the LiCl alone, (c) the pairing of mint and LiCl on the day of conditioning, and (d) the reexposure to mint after an earlier pairing of mint and LiCl. These experiments provide clear evidence that rat fetuses are capable of forming conditioned taste/odor aversions as early as Day 17 of gestation and, further, that rat fetuses are capable of expressing these learned aversions in utero.

In utero chemosensory experience alters taste preferences and corticosterone responsiveness.

Litters of rat pups were exposed in utero (on Day 20 of gestation) to taste/odor stimulation by injection of an apple juice solution into the amniotic fluid. One group of control litters was exposed to a saline solution while a second control group received a sham-injection treatment. All litters were delivered by cesarean section and fostered to females that had given birth to a litter normally. Offspring were tested as adults in one of two two-bottle preference tests (apple solution vs tap water or maple solution vs tap water). Measures of total fluid consumption were converted to preference scores and plasma levels of corticosterone were determined. Analyses of these data indicated that offspring exposed to the apple solution in utero showed an increased preference for apple postnatally. No increased preference for maple solution was shown. In both preference tests the offspring exposed to apple or saline solutions via amniotic injection had reduced pituitary-adrenal activity compared to sham-injected controls. The results are compared to findings of other studies of pre- and postnatal stimulation on offspring behavior and pituitary-adrenal activity.

Environmental determinants of behaviour in the rat fetus

Abstract Using a preparation which allows in vivo observation, the spontaneous behaviour of rat fetuses was recorded on successive days during the last third of gestation (days 16–21) in each of three microenviroments: In Uterus (viewed through the uterine wall), In Amnion (delivered outside the uterus and viewed through the intact amniotic membranes), and In Bath (removed from both uterus and amnion into a benign fluid medium with placental connection intact). These observations provide evidence that the rat fetus exhibits ontogenetic changes in behavioural repertoire, diversity and organization and is reponsive to variations within its environment as development proceeds.

Prenatal Expression of Species-Typical Action Patterns in the Rat Fetus (Rattus norvegicus)

We investigated sensory and behavioral responsiveness of the rat fetus. On Days 19, 20, or 21 of gestation, rat fetuses received intraoral infusions of a biologically important stimulus, milk, or a novel chemical stimulus, lemon. Using a technique to directly observe behavior in utero, we found that rat fetuses discriminate between intraoral infusions of milk and lemon, exhibiting different levels and patterns of overall activity after infusion. Milk was found to evoke a low magnitude, delayed increase in overall fetal activity from Day 19 through Day 21, whereas lemon evoked a high-magnitude, spiked pattern of activity that diminished from Day 19 to Day 21. Late in gestation these two stimuli elicited species-typical action patterns. Milk infusions elicited a stretch response much like the one shown by pups at the nipple; lemon infusions elicited face wiping typical of older pups and adults exposed to aversive gustatory stimuli.

Behavior of rat fetuses following chemical or tactile stimulation

The behavior of fetal rats was examined on Day 19 of gestation with procedures that enabled chemical stimulation and direct observation of fetuses. Rat fetuses are sensitive to both tactile stroking and intraoral infusion of chemical solutions, but the pattern and amount of activity depend upon the modality of stimulation. Fetal responsiveness is affected by prior experience with chemical stimuli. Repeated exposure within a 10-min period results in a waning of response, and repeated exposure across a delay of 48 hr results in a different pattern of response than is seen to a novel stimulus. Reexposure to a stimulus experienced earlier in gestation also alters fetal responsiveness to other forms of tactile and chemical stimulation. These findings indicate that the rat fetus exhibits olfactory function in utero and suggest central processing of sensory information, including evidence of habituation, a fetal orienting reflex to novel stimuli, and the existence of prenatal behavioral states associated with different patterns of response.

The Prenatal Origins of Behavioral Organization

Recognition that organisms have a developmental history, exhibit behavior that is uniquely suited to or constrained by features of their immediate environment, and adapt to new environments is central to current psychobiological thought. Unfortunately, these concepts have in the past been restricted largely to the study of postnatal behavioral development. However, recent extension of these concepts to the fetus as an active and interactive organism that resides within a specialized, intrauterine niche is proving to be a profitable approach toward understanding the origins of behavioral organization during development.

Environmental determinants of behaviour in the rat fetus. II. The emergence of synchronous movement

Abstract Rat fetuses were observed directly in different micro-environments (in utero and ex utero) on successive days during the last third of gestation. Synchronous movements comprising two or more regions of the body became common on day 17 of gestation and were especially prevalent ex utero. Their occurrence could not be explained satisfactorily by a stochastic model involving chance association of individual body regions. If synchronized movements are considered as evidence of behavioural organization, then fetal behaviour appears more diverse than previously recognized and exhibits specific linkages between body regions that imply emergent coordination and the prenatal development of species-typical action patterns.

Cryptopsychobiology: the appearance, disappearance, and reappearance of a species-typical action pattern during early development.

Late in gestation, intraoral infusion of lemon elicits a facial wiping response from rat fetuses. This facial wiping response is isomorphic with that of older pups and adult rats exposed to aversive oral stimulation. Most studies of the postnatal development of aversive responses have demonstrated that facial wiping does not appear in the repertoire of rat pups until the second postnatal week. In certain test situations, however, wiping can be elicited from neonatal rats. This fact suggests that the expression of facial wiping by neonates is constrained or facilitated by the environmental conditions present at the time of testing. In this report, a series of seven experiments is described that document the wiping response of rat fetuses and pups in age-typical environments, and an environmental constraint hypothesis is examined. Examination of the ontogeny of facial wiping in this manner highlights issues that should be addressed in studies of behavioral continuity between the prenatal and the postnatal periods.