Behavioral Neuroscience Copyright 1988 by the American Psychological Association, Inc. 1988, Vol. 102, No. 1, 24-34 0735-7044/88/$00.75 Behavior of Rat Fetuses Following Chemical or Tactile Stimulation William P. Smotherman and Scott R. Robinson Departments of Psychology and Zoology, Oregon State University 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 fetus develops within a complex intrauterine environ- ment that changes over the course of gestation. Within the uterus fetuses are exposed to a diverse assortment of stimuli, including mechanical stimuli originating in the outside world or maternal physiology and a rich chemical milieu that varies with alterations in maternal diet or environment (Smother- man & Robinson, in press). Because the fetal environment is variable, sensory responsiveness might be anticipated as a normal feature of prenatal behavioral development. Indeed, there is growing evidence that fetuses are sensitive to intra- uterine stimuli and can modify their behavior in response to stimulation (Smotherman & Robinson, 1987). Fetuses are active in utero and exhibit a behavioral reper- toire that expands up to the time of birth (de Vries, Visser, & Prechtl, 1982; Robinson & Smotherman, 1987; Smotherman & Robinson, 1986). Fetal activity is both complex and orga- nized, showing temporal patterning (Smotherman & Robin- son, 1986), rhythmicity (Robertson, 1985), synchrony (Ro- binson & Smotherman, 1987), and emergent coordination (Bekoff & Lau, 1980). Fetuses are also responsive to altera- tions in their immediate physical environment, becoming more active outside the restraining influence of the uterus and amniotic sac than in utero (Smotherman & Robinson, 1986). The behavioral sophistication evident in these findings argues that spontaneous fetal activity cannot be characterized, as it has been in the past, as random motility bearing little relation to postnatal behavior (Hamburger, 1963). Earnest inquiry into the prenatal roots of responsive behav- ior began in the 1920s and '30s (Angulo y Gonzalez, 1932; Barcroft & Barron, 1939; Carmichael, 1934; Coghill, 1929; This research was supported by National Institute of Child Health and Human Development Grant HD 16102-05 and Research Career Development Award HD 00719-01 to W. P. Smotherman. We thank Patricia La Vallee for technical assistance in this study. Correspondence concerning this article should be addressed to W. P. Smotherman, Laboratory for Psychobiological Research, Depart- ment of Psychology, Oregon State University, Corvallis, Oregon 97331. 24 Windle & Griffin, 1931). These early students were primarily interested in neurological development and exploited fetal behavior as a means of charting the emergence of spinal reflexes. Toward this end, methods were developed for pre- senting tactile stimulation by probing or stroking fetuses in utero. Probing the skin of fetal rats with a stiff bristle or pin has enabled the mapping of body regions sensitive to punctate tactile stimuli (Narayanan, Fox, & Hamburger, 1971). Fetuses are indeed responsive to tactile stimulation, exhibiting both local reflexes and more general activity. It is interesting that the perioral region is among the earliest to become sensitive to tactile stimulation and remains consistently sensitive throughout gestation. In contrast to the early investigation of tactile stimuli, prenatal responsiveness to tastes and odors has only recently come under scrutiny with the advent of techniques for deliv- ering chemical solutions into the amniotic fluid of the devel- oping rat fetus (Blass & Pedersen, 1980; Stickrod, 1981). Studies of labeled glucose uptake in the accessory olfactory bulbs of fetal rats indicate that the olfactory system is func- tional before birth (Mistretta & Bradley, 1986; Pedersen, Stewart, Greer, & Shepherd, 1983). This finding agrees with behavioral evidence that neonatal rats are sensitive to odor cues that they experience in utero (Pedersen & Blass, 1982; Smotherman, 1982a). Early postnatal behavior, such as suck- ling, seems dependent upon olfactory stimuli. The cue that orients the rat pup to the nipple for the first suckling episode is a substance (olfactorant) present in the amniotic fluid (Pedersen & Blass, 1981). Manipulation of the prenatal chemical environment also has provided direct evidence that fetuses are capable of asso- ciating neutral chemical cues with aversive stimulation in utero. It is well known that in adult rats the conjunction of a taste or odor with a noxious chemical (ip injection of lithium chloride) leads to the formation of a conditioned aversion (Garcia, Lasiter, Bermudez-Ratoni, & Deems, 1985). Condi- tioning of this kind can be acquired in utero by the rat fetus and expressed as altered behavior during either the prenatal or the postnatal period. For example, rat fetuses conditioned