Purpose: The behavior of the human fetus consists of complex dynamic relationships. To date, previous methods of measuring fetal behavior have failed to capture the complexity of behavior. However, as behavior is a reflection of neural functioning it is only when quantitative assessment of this complexity has been undertaken that underlying neural organization can be elucidated. In order to reveal fundamental features of neurobehavioral organization and development, the present study provided a quantitative description of the complex spatial (sequential) and temporal (synchronous and asynchronous) patterning of behavior in the human fetus in early pregnancy.Methods: Twenty fetuses from normal singleton pregnancies were scanned at two weekly intervals for a period of 1 h from 9 to 17 weeks' gestation. An ethogram of the timing and sequencing of right and left arm and leg movements was constructed from each videotaped session. A description of sequential and synchronous relationships between limb movements was determined using stochastic modeling. The temporal patterning of activity in arm, leg and all limb movements was examined by quantitatively determining bout criterion using survivor analysis.Results: Fetuses exhibited within and between limb synchronous, sequential and temporal patterning from the appearance of single limb movements indicating that initial patterning may be genetically hard‐wired. Self‐organization of behavior was apparent in increasing synchronous, sequential and temporal patterning with advancing gestation. These changes coincided with rapid increases in neurulation, synaptogenesis and myelinization in early pregnancy. Different sequential, synchronous and temporal organization was found in arm and leg movements indicating differential neural control of co‐ordination in these limbs. Furthermore, lateralization and gender differences were found to be important features of behavioral organization.Conclusions: The present study has revealed that quantitative assessment can define and measure behavioral complexity and this can elucidate fundamental neurobehavioral organization in early pregnancy.

Fetuses of diabetic mothers exhibit maturational delays in their behaviour and disturbances in behavioural and intellectual functioning in childhood. This suggests an effect of maternal diabetes on the central nervous system of the fetus. The habituation technique enables the functioning of the higher central nervous system to be examined. A normal habituation pattern reflects an intact central nervous system. Previous studies have found abnormalities in the fetal central nervous system are reflected in habituation performance. This paper examined the habituation ability of fetuses of diabetic mothers and of non-diabetic mothers. The fetuses were tested at 28, 32 and 36 weeks of gestation. After 2 min of fetal inactivity a series of vibroacoustic stimuli were presented to the fetus. This continued until no response was observed on five consecutive stimulus presentations. The number of stimulus presentations to habituate at each gestational age was recorded. The results reveal that there was a highly significant main effect of group (F(1,47)=19.65, P<0.001). Fetuses of diabetic pregnancies took longer to habituate. There was a significant effect of gestational age (F(2,94)=44.67, P<0.0001). In both groups the number of trials to habituate decreased with advancing gestation. There was no relationship between random blood glucose levels and habituation performance. The results demonstrate that maternal diabetes affects higher aspects of central nervous system functioning in the fetus.

BackgroundChildren with specific reading difficulties have problems that extend beyond the range of underlying language-related deficits (eg, they have difficulties with balance and motor control). We investigated the role of persistent primary reflexes (which are closely linked in the earliest months of life to the balance system) in disrupting the development of reading skills.MethodsWe assessed the efficacy of an intervention programme based on replicating the movements generated by the primary-reflex system during fetal and neonatal life. A randomised, individually matched, double-blind, placebo-controlled design was used and children (aged 8–11 years) with persistent primary reflexes and a poor standard of reading were enrolled into one of three treatment groups: experimental (children were given a specific movement sequence); placebo-control (children were given non-specific movements); and control (no movements).FindingsFrom an initial sample of 98 children, 60 children, 20 in each group were matched on age, sex, verbal intelligence quotient (IQ), reading ability, and persistent asymmetrical tonic neck reflex. For asymmetrical tonic neck-reflex levels there was a significant (group by time) interaction (p<0·001). The experimental group showed a significant decrease in the level of persistent reflex over the course of the study (mean change -1·8 [95% CI -2·4 to -1·2], p<0·001), whereas the changes in the placebo-control and control groups were not significant (-0·2 [-0·9 to 0·6] and -0·4 [-0·9 to 0·2]).InterpretationThis study provides further evidence of a link between reading difficulties and control of movement in children. In particular, our study highlights how the educational functioning of children may be linked to interference from an early neurodevelopmental system (the primary-reflex system). A new approach to the treatment of children with reading difficulties is proposed involving assessment of underlying neurological functioning, and appropriate remediation.

Behavioural lateralisation is a common feature of everyday behaviour, most familiar in the exhibition of handedness. Despite differing theories about the origins of laterality, little is known about their ontogenesis. This study observed the left and right arm movements of 72 foetuses at 10 weeks of gestational age, the first age at which lateralised behaviour may be observed. There was a highly significant preference for foetuses to move their right arm more than their left arm, 85% exhibiting more right arm than left arm movements. There was no difference in the amount of movements exhibited with the preferred arm, whether it be right or left. Laterality of behaviour at such an early gestational age (probably as early as it is possible for it to be observed) is unlikely to be under brain control but is probably of more muscular or spinal determination. The possibility that early differential motor behaviour may contribute to subsequent laterality of behaviour and asymmetrical brain growth, must be considered.

Developmental Medicine & Child NeurologyVolume 39, Issue 5 p. 343-346 Free Access Memory in utero ? Peter G. Hepper, Peter G. Hepper Foetal Behaviour Research Centre, School of Psychology, Queens University, Belfast BT7 IXX, X Ireland, UKSearch for more papers by this author Peter G. Hepper, Peter G. Hepper Foetal Behaviour Research Centre, School of Psychology, Queens University, Belfast BT7 IXX, X Ireland, UKSearch for more papers by this author First published: 29 September 2008 https://doi.org/10.1111/j.1469-8749.1997.tb07442.xCitations: 11AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Citing Literature Volume39, Issue5May 1997Pages 343-346 ReferencesRelatedInformation

Ultrasound in Obstetrics & GynecologyVolume 8, Issue 3 p. 145-148 EditorialFree Access Fetal behavior: why so sceptical? Peter G. Hepper, Peter G. Hepper Fetal Behaviour Research Centre, School of Psychology, Queen's University of Belfast, Northern IrelandSearch for more papers by this author Peter G. Hepper, Peter G. Hepper Fetal Behaviour Research Centre, School of Psychology, Queen's University of Belfast, Northern IrelandSearch for more papers by this author First published: 1 September 1996 https://doi.org/10.1046/j.1469-0705.1996.08030145.xCitations: 25AboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Citing Literature Volume8, Issue31 September 1996Pages 145-148 RelatedInformation

Whether fetal memory exists has attracted interest for many thousands of years. The following review draws on recent experimental evidence to consider two questions: does the fetus have a memory? And, if so, what function(s) does it serve? Evidence from fetal learning paradigms of classical conditioning, habituation and exposure learning reveal that the fetus does have a memory. By comparison little attention has been paid to the possible function of memory. Possible functions discussed are: practice, recognition of and attachment to the mother, promotion of breastfeeding, and language acquisition. It is concluded that the fetus does possess a memory but that more attention to the functions of fetal memory will guide future studies of fetal memory abilities.

This paper reports a series of ultrasound observations on a human fetus from 21 weeks of gestational age at two weekly intervals to term. The mother, until 18 weeks of gestational age, was a user of cocaine but after this age used cocaine only once at 31 weeks gestation. The behaviour of this fetus was compared to a group of 10 similar aged fetuses who were not exposed to cocaine. Exposure to cocaine resulted in prolonged periods of inactivity interspersed with periods of increased general activity and an increased number of startles. This was particularly evident immediately following exposure to cocaine but behaviour appeared to become more normal with time as the mother stopped using cocaine. The behavioural states of the cocaine exposed fetus were different from unexposed fetuses. Longer periods were spent in States 1F and 4F and less time in State 2F. Furthermore the incidence of periods where no states were observed was considerably higher. These observations demonstrate that maternal cocaine use disrupts the behaviour of the fetus indicating a direct effect on the CNS. The value of prenatal behavioural observations to assess the effects of neurotoxic agents is demonstrated.

Previous research has revealed that the human fetus responds to sound, but to date there has been little systematic investigation of the development of fetal hearing. The development of fetal behavioural responsiveness to pure tone auditory stimuli (100 Hz, 250 Hz, 500 Hz, 1000 Hz, and 3000 Hz) was examined from 19 to 35 weeks of gestational age. Stimuli were presented by a loudspeaker placed on the maternal abdomen and the fetus's response, a movement, recorded by ultrasound. The fetus responded first to the 500 Hz tone, where the first response was observed at 19 weeks of gestational age. The range of frequencies responded to expanded first downwards to lower frequencies, 100 Hz and 250 Hz, and then upwards to higher frequencies, 1000 Hz and 3000 Hz. At 27 weeks of gestational age, 96% of fetuses responded to the 250 Hz and 500 Hz tones but none responded to the 1000 Hz and 3000 Hz tones. Responsiveness to 1000 Hz and 3000 Hz tones was observed in all fetuses at 33 and 35 weeks of gestational age, respectively. For all frequencies there was a large decrease (20-30 dB) in the intensity level required to elicit a response as the fetus matured. The observed pattern of behavioural responsiveness reflects underlying maturation of the auditory system. The sensitivity of the fetus to sounds in the low frequency range may promote language acquisition and result in increased susceptibility to auditory system damage arising from exposure to intense low frequency sounds.

The ability to discriminate between acoustic signals of different frequencies is fundamental to the interpretation of auditory information and the development of language perception and production. The fact that the human fetus responds to sounds of different frequencies raises the question of whether the fetus is able to discriminate between them? To investigate whether the fetus has the ability to discriminate between different pure tone acoustic stimuli and different speech sounds the following study used an habituation paradigm and examined whether the fetus could discriminate between two pure tone acoustic stimuli, 250 Hz and 500 Hz, or two speech sounds, [ba] and [bi], at 27 and 35 weeks of gestational age. The results indicated that the fetus is capable of discriminating between the different sounds, i.e. 250 Hz and 500 Hz and [ba] and [bi] at 35 weeks of gestational age but less able at 27 weeks of gestational age. The implications of this for the development of the auditory system are discussed.

The intrauterine environment presents a rich array of sensory stimuli to which the fetus responds. The maternal voice is perhaps the most salient of all auditory stimuli. The following experiments examined the movement response of the fetus and newborn to its mother's voice and a strange female's voice and to voices speaking normally and speaking 'motherese'. Newborns (2-4 days of age) discriminated, as measured by the number of movements exhibited to the presentation of the stimuli, between their mother's voice and a stranger's voice and between normal speech and 'motherese', in both cases the former being preferred. Fetuses, 36 weeks of gestational age, evidenced no ability to discriminate between their mother's and a stranger's voice played to them via a loudspeaker on the abdomen but did discriminate between their mother's voice when played to them by a loudspeaker on the abdomen and the mother's voice produced by her speaking. The results are further evidence of the ability of the fetus to learn prenatally and indicate a possible role for prenatal experience of voices in subsequent language development and attachment.

In this experiment, fetal rats, Rattus norvegicus, were subjected to a single transient hypoxic episode before an injection of orange essence or isotonic saline through the uterine and amniotic membranes into the amniotic fluid within 5 s of the release from hypoxia. Other animals experienced either orange essence or isotonic saline alone following no hypoxic episode. At 120 days after birth, adult rats were given a two-choice preference test between orange and water. Only those animals who experienced the orange following release from hypoxia showed a preference for the orange. These results suggest that the acquired preference is not a result of simple exposure but is suggestive of a role for reoxygenation as a positive reinforcer.

Since 1981, when eye movements of the human fetus were first reported the study of fetal eye movements has increased, mainly focusing on the ontogenesis of eye movements and as one parameter of behavioral states. Using real-time ultrasound fetal eye movements can be clearly observed from 14 weeks of gestational age. Fetal eye movements may be described in terms of their pattern, frequency and incidence of periods containing eye movements and no eye movements. Furthermore, the relationship of eye movements to other behaviors may be used to give information on the integration of central nervous system function. A picture of normal fetal eye movements can be constructed and used to detect abnormalities in eye movements which can indicate underlying abnormalities of the central nervous system. This paper concludes that, although in its early stages, the study of fetal eye movements holds promise for a greater understanding of brain development and the assessment of the condition of the fetus.

The ability of ten normal and two Down's syndrome fetuses to habituate to a repeated auditory stimulus was assessed. The normal fetuses were assessed on two separate occasions during the final trimester of pregnancy. The number of trials to habituate and latency to respond were recorded. The results demonstrated that all normal fetuses exhibited a decrement in response to repeated presentations of the stimulus, a 250-Hz sine wave. This was the result of habituation and not fatigue since fetuses recovered responding upon presentation of a new (500 Hz) stimulus and habituated faster on re-presentation of the original stimulus. The performance of fetuses remained stable over the two testing periods. The response of the Down's syndrome fetuses was different to that of normal fetuses rarely overlapping indices of habituation exhibited by normal fetuses. The study concludes that habituation may be a powerful tool to examine the behavioural and sensory development of the fetus and may be of use in the antenatal assessment of the existence and severity of neural abnormality.

The behaviour of 5 fetuses at 10 weeks of gestational age that later underwent a spontaneous abortion during the first trimester of pregnancy was compared to similar aged normal fetuses (n = 116). Marked abnormalities of behaviour were noted in three of the pregnancies that spontaneously aborted. These behavioural abnormalities were not identified in any of the pregnancies which continued to term. We conclude that fetal behaviour, which reflects the neural integrity of the individual, and thus fetal well-being, can be used during the first trimester to give an indication as to the viability of the on-going pregnancy.

We examined the effect of embryonic olfactory experiences on behaviour after hatching in two species of anuran amphibians, Rana temporaria and Rana sylvatica. Odorants (orange and citral) injected into the egg were "learned" by the' embryo and subsequently preferred by tadpoles after hatching. The observed preferences were specific to the odours experienced prior to hatching, and tadpoles discriminated between the odour experienced as embryos and a novel odour. The acquired preference was maintained after metamorphosis for those individuals that exhibited a preference as tadpoles. Preferences of tadpoles were also influenced "naturally" by odours present in the water surrounding the developing embryos. The experimentally induced olfactory preferences did not appear to influence the exhibition of sibling recognition abilities. The study represents the first demonstration of "embryonic" learning in amphibians, and the functions and importance of early olfactory learning for amphibians are discussed.

A behavioral and structural analysis using ultrasound of a fetus suffering from Edwards syndrome is described. A number of structural anomalies were observed: the classic hand deformity, extended legs, diamond-shaped head, open mouth and a severe cardiac abnormality. A number of distinctive behavior patterns were observed: vertical eye movements, longitudinal rotation of the trunk, rotation of hands, tremor of extremities and pulsatile body movements, which are not usually seen in the normal fetus. The use of behavioral indicators in the diagnosis of abnormalities is discussed. We conclude that the analysis of behavior may make a significant contribution to the ultrasonographic diagnosis of handicap.

The developmental origins of behavioural asymmetries. in particular handedness. have aroused considerable interest and debate. Until now such behavioural asymmetries have only been reported after birth. Here we report the existence of handedness before birth. expressed in terms of thumb-sucking by the fetus. Ultrasound observations of fetuses from 15 weeks to term revealed a marked bias for sucking the thumb of the right hand. This preference appears to be maintained throughout pregnancy, is unrelated to fetal position in utero but correlates with head position preference in the supine newborn. The findings indicate that handedness is present prior to birth and the implications of this for the development of laterality are discussed.