Early Environmental Experience Research Articles

Distinct aspects of the early environment contribute to associative memory, cued attention, and memory-guided attention: Implications for academic achievement

Childhood socioeconomic status (SES) is associated with numerous aspects of cognitive development and disparities in academic achievement. The specific environmental factors that contribute to these disparities remain poorly understood. We used observational methods to characterize three aspects of the early environment that may contribute to SES-related differences in cognitive development: violence exposure, cognitive stimulation, and quality of the physical environment. We evaluated the associations of these environmental characteristics with associative memory, cued attention, and memory-guided attention in a sample of 101 children aged 60–75 months. We further investigated whether these specific cognitive abilities mediated the association between SES and academic achievement 18 months later. Violence exposure was specifically associated with poor associative memory, but not cued attention or memory-guided attention. Cognitive stimulation and higher quality physical environment were positively associated with cued attention accuracy, but not after adjusting for all other environmental variables. The quality of the physical environment was associated with memory-guided attention accuracy. Of the cognitive abilities examined, only memory-guided attention contributed to SES-related differences in academic achievement. These findings suggest specificity in how particular aspects of early environmental experience scaffold different types of attention and memory subserved by distinct neural circuits and shed light on a novel cognitive-developmental mechanism underlying SES-related disparities in academic achievement.

Early experiences mediate distinct adult gene expression and reproductive programs in Caenorhabditis elegans.

Environmental stress during early development in animals can have profound effects on adult phenotypes via programmed changes in gene expression. Using the nematode C. elegans, we demonstrated previously that adults retain a cellular memory of their developmental experience that is manifested by differences in gene expression and life history traits; however, the sophistication of this system in response to different environmental stresses, and how it dictates phenotypic plasticity in adults that contribute to increased fitness in response to distinct environmental challenges, was unknown. Using transcriptional profiling, we show here that C. elegans adults indeed retain distinct cellular memories of different environmental conditions. We identified approximately 500 genes in adults that entered dauer due to starvation that exhibit significant opposite (“seesaw”) transcriptional phenotypes compared to adults that entered dauer due to crowding, and are distinct from animals that bypassed dauer. Moreover, we show that two-thirds of the genes in the genome experience a 2-fold or greater seesaw trend in gene expression, and based upon the direction of change, are enriched in large, tightly linked regions on different chromosomes. Importantly, these transcriptional programs correspond to significant changes in brood size depending on the experienced stress. In addition, we demonstrate that while the observed seesaw gene expression changes occur in both somatic and germline tissue, only starvation-induced changes require a functional GLP-4 protein necessary for germline development, and both programs require the Argonaute CSR-1. Thus, our results suggest that signaling between the soma and the germ line can generate phenotypic plasticity as a result of early environmental experience, and likely contribute to increased fitness in adverse conditions and the evolution of the C. elegans genome.

Oxytocin receptor gene polymorphisms (rs53576) and early paternal care sensitize males to distressing female vocalizations.

The oxytocinergic system is highly involved in social bonding and early caregiver-infant interactions. Here, we hypothesize that oxytocin receptor (OXTR) gene genotype and parental bonding history interact in influencing social development. To address this question, we assessed adult males' arousal (heart rate changes) in response to different distress vocalizations (human female, human infant and bonobo). Region rs53576 of the OXTR gene was genotyped from buccal mucosa cell samples, and a self-report Parental Bonding Instrument was used (which provide information about parental care or parental overprotection). A significant gene-environment interaction between OXTR genotype and parenting style was found to influence participants' social responsivity to female cry vocalizations. Specifically, a history of appropriate paternal care in participants accentuated the heightened social sensitivity determined by G/G homozygosity, while higher versus lower paternal overprotection lead to distinct levels of physiological arousal particularly in A carriers individuals. These results add to our understanding of the dynamic interplay between genetic susceptibility and early environmental experience in shaping the development of appropriate social sensitivity in males.

Early experiences can alter the size of cortical fields in prairie voles (Microtus ochrogaster).

The neocortex of the prairie vole is composed of three well-defined sensory areas and one motor area: primary somatosensory, visual, auditory areas, and the primary motor area, respectively. The boundaries of these cortical areas are identifiable very early in development, and have been thought to resist alteration by all but the most extreme physical or genetic manipulations. Here we assessed the extent to which the boundaries of sensory/motor cortical areas can be altered by exposing young prairie voles ( Microtus ochrogaster ) to a chronic stimulus, high or low levels of parental contact, or an acute stimulus, a single dose of saline, oxytocin (OT), or oxytocin antagonist on the day of birth. When animals reached adulthood, their brains were removed, the cortex was flattened, cut parallel to the pial surface, and stained for myelin to identify the architectonic boundaries of sensory and motor areas. We measured the overall proportion of cortex that was myelinated, as well as the proportion of cortex devoted to the sensory and motor areas. Both the chronic and acute manipulations were linked to significant alterations in areal boundaries of cortical fields, but the areas affected differed with different conditions. Thus, differences in parental care and early exposure to OT can both change cortical organization, but their effects are not identical. Furthermore, the effects of both manipulations were sexually dimorphic, with a greater number of statistically significant differences in females than in males. These results indicate that early environmental experience, both through exposure to exogenous neuropeptides and parental contact can alter the size of cortical fields.

Unpredictability in food supply during early life influences growth and boldness in European seabass, Dicentrarchus labrax

Biological variability is no longer considered as statistical noise, but rather as an adaptive benefit. This variability comes from consistent differences in behavioral and physiological responses among individuals to a changing/challenging environment, named “coping style”, “temperament” or “personality”. Many studies have described how to characterize personality traits and how to assess their consistency over time and between different contexts; however, little is known about the environmental factors shaping personality development. Because contrasting personalities are maintained with evolution, this lead to the widespread assumption that genes play a predominant role in personality. In many cases, personality traits are however also likely to be determined by individual experience, which is probably at least as important as genetics in shaping personality. The aim of this study was to assess how environmental variability (herein food predictability) impacts behavioral responses, particularly the shyness-boldness axis, one of the most widely shared animal personality trait. Here, we reared juvenile seabass (95days old) from two divergent strains selected for feed deprivation tolerance under standard conditions for 40days. Thereafter, we submitted them to two feeding treatments (Predictable versus Unpredictable) starting at 135 dph and lasting 60days. Seabass reared under a predictable food supply (PFS) grew faster and were shyer than fish reared under an unpredictable food supply (UFS) (i.e. they took more time to exit the refuge zone of a Z-maze; UFS: 132.47±34.63s; PFS: 336.79±56.97s) but their exploration tendency was similar. We also examined the behavioral responses of these fish facing a hypoxic challenge. Hypoxia tolerance results were consistent before and after the two feeding treatments. Our findings show the importance of early environmental experience as a driving force shaping boldness. In addition, we provide further evidence that predictable feeding time should be respected in studies assessing essential functions such as growth and behavior. Although personality traits are partially heritable, this study demonstrates the important influence of environmental conditions and life history on behavior.

Adverse Childhood Events and Psychosis in Bipolar Affective Disorder

Background There has been increasing interest in the association between childhood trauma and psychosis. Proposals for potential mechanisms involved include affective dysregulation and appraisals of threat, yet few large-scale clinical studies exist in affective psychosis. Aim We hypothesise that within bipolar disorder (BD), childhood events will show a significant association with psychosis, and in particular with symptoms driven by dysregulation of mood or with a persecutory content. Method 2019 participants were recruited as part of our programme of research into the genetic and non-genetic determinants of BD ( www.bdrn.org ). Data on lifetime ever presence of psychosis and specific psychotic symptoms were determined by detailed structured interview with case note review. Childhood events were recorded after self-report questionnaire and case note information. Results There was no relationship between childhood events, or childhood abuse, and psychosis per se. Childhood events were not associated with increased risk of persecutory or other delusions. Significant associations were found between childhood abuse and auditory hallucinations, strongest between sexual abuse and mood congruent or abusive voices. These relationships remain significant after controlling for lifetime ever cannabis misuse. Conclusions Within affective disorder, the relationship between childhood events and psychosis appears to be relatively symptom-specific. It is possible that the pathways leading to psychotic symptoms differ, with delusions and non-hallucinatory symptoms being influenced less by childhood or early environmental experience. 1. Upthegrove R, Chard C, Jones, L, Gordon –Smith K, Forty L, Jones I and Craddock N. Adverse Childhood Events and Psychosis in Bipolar Affective Disorder. BJPsych In press BJP/2014/152611

Adverse childhood events and psychosis in bipolar affective disorder

There has been increasing interest in the association between childhood trauma and psychosis. Proposals for potential mechanisms involved include affective dysregulation and cognitive appraisals of threat. To establish if, within bipolar disorder, childhood events show a significant association with psychosis, and in particular with symptoms driven by dysregulation of mood or with a persecutory content. Data on lifetime-ever presence of psychotic symptoms were determined by detailed structured interview with case-note review (n = 2019). Childhood events were recorded using a self-report questionnaire and case-note information. There was no relationship between childhood events, or childhood abuse, and psychosis per se. Childhood events were not associated with an increased risk of persecutory or other delusions. Significant associations were found between childhood abuse and auditory hallucinations, strongest between sexual abuse and mood congruent or abusive voices. These relationships remain significant even after controlling for lifetime-ever cannabis misuse. Within affective disorder, the relationship between childhood events and psychosis appears to be relatively symptom-specific. It is possible that the pathways leading to psychotic symptoms differ, with delusions and non-hallucinatory symptoms being influenced less by childhood or early environmental experience.

Maternal genotype influences behavioral development of 3×Tg-AD mouse pups

Transgenic mice are a valuable tool in the investigation of neurodegenerative disorders such as Alzheimer's disease. The triple transgenic mouse (3×Tg-AD) is a model of Alzheimer's disease that possesses age-related amyloid beta plaques, neurofibrillary tangles and cell death as well as cognitive decline. Because maternal effects may interact with pup genotype in determining behavior phenotypes, we used a cross-fostering paradigm to investigate the effects of maternal genotype on behavioral development of the 3×Tg-AD mouse model and its wildtype control (B6129S1F2) from 2 to 24 days of age. Developmental patterns of behavior were influenced by both pup and maternal genotype. The 3×Tg-AD mice were delayed in sensory reflexes, showed less activity and poorer habituation to a novel object, but showed advanced development of motor reflexes compared to wildtype pups. While there were no differences in levels of maternal care between transgenic and control mothers, maternal genotype affected the development of several pup reflexes (body weight, hindlimb grasp reflex, loss of crossed extensor reflex, vibrissae response, righting reflex) and the number of horizontal and vertical beam breaks in an open field. This study is the first to examine neurobehavioral development and maternal behavior in a mouse model of Alzheimer's disease, and highlights the importance of investigating the consequences of early environmental experience as well as genetic manipulation on behavioral development.

Parent–infant interaction in infant siblings at risk of autism

Recent models of the early emergence of autism spectrum disorder (ASD) propose an interaction between risk susceptibility and the infant's social environment, resulting in a progressively atypical developmental trajectory. The infant's early social environmental experience consists mostly of interaction with caregivers, yet there has been little systematic study of early parent-infant interaction in infants at risk of ASD. This study examined the global characteristics of parent-infant interaction in 6- to 10-month-old infants with an older sibling diagnosed with ASD (at-risk sibs), in comparison with a group of infants with no family history of ASD (low-risk sibs). As part of the British Autism Study of Infant Siblings (BASIS), 6-min videotaped unstructured play interactions of mother-infant dyads (45 at-risk sibs and 47 low-risk sibs) were rated on global aspects of parent-infant interaction, blind to participant information. Differences in global characteristics of interaction were observed in both infant and parent contributions in the at-risk group compared to low-risk controls. In analyses adjusted for age and developmental level, at-risk sib infants were less lively, and their parents showed higher directiveness, and lower sensitive responding (as a trend after adjustment). Level of infant liveliness was independent of other interactive behaviour. Consistent with reports in previous literature in older children with autism and in other neurodevelopmental disorders, our findings may suggest that infants at genetic risk are exposed to a more directive interactive style relatively early in infancy. We discuss possible explanations for these findings and implications for further developmental study and intervention.

Juvenile exposure to predator cues induces a larger egg size in fish

When females anticipate a hazardous environment for their offspring, they can increase offspring survival by producing larger young. Early environmental experience determines egg size in different animal taxa. We predicted that a higher perceived predation risk by juveniles would cause an increase in the sizes of eggs that they produce as adults. To test this, we exposed juveniles of the mouthbrooding cichlid Eretmodus cyanostictus in a split-brood experiment either to cues of a natural predator or to a control situation. After maturation, females that had been confronted with predators produced heavier eggs, whereas clutch size itself was not affected by the treatment. This effect cannot be explained by a differential female body size because the predator treatment did not influence growth trajectories. The observed increase of egg mass is likely to be adaptive, as heavier eggs gave rise to larger young and in fish, juvenile predation risk drops sharply with increasing body size. This study provides the first evidence that predator cues perceived by females early in life positively affect egg mass, suggesting that these cues allow her to predict the predation risk for her offspring.

A Cellular Memory of Developmental History Generates Phenotypic Diversity in C. elegans

Early life experiences have a major impact on adult phenotypes [1-3]. However, the mechanisms by which animals retain a cellular memory of early experience are not well understood. Here we show that adult wild-type Caenorhabditis elegans that transiently pass through the stress-resistant dauer larval stage exhibit distinct gene expression profiles and life history traits, as compared to adult animals that bypassed this stage. Using chromatin immunoprecipitation experiments coupled with massively parallel sequencing, we found that genome-wide levels of specific histone tail modifications are markedly altered in postdauer animals. Mutations in subsets of genes implicated in chromatin remodeling abolish, or alter, the observed changes in gene expression and life history traits in postdauer animals. Modifications to the epigenome as a consequence of early experience may contribute in part to a memory of early experience and generate phenotypic variation in an isogenic population.

Early environmental experience alters baseline and ethanol-induced cognitive impulsivity: relationship to forebrain 5-HT 1A receptor binding

The relationship between impulsivity and drug abuse is poorly understood despite evidence that impulsive behaviour both predicts, and is a consequence of, drug use. Moreover, although there are clear individual differences in the propensity to addiction, this relationship has not been investigated with respect to impulsive behaviour. We tested whether early environmental experience would influence behavioural measures of impulsivity, and further, whether this experience would alter impulsive choice following ethanol intoxication. Thirty-six male, Long-Evans rats were reared in either isolated (1 rat/cage), standard (2 rats/cage), or enriched (group housed with toys) conditions. After a 3-month rearing period, animals were tested in two operant tasks measuring either motor (go/no-go) or cognitive (delay-to-reinforcement) impulsivity. Rats were then re-tested following 0, 0.3, 0.6, 0.9, and 1.2 g/kg ethanol. Forebrain 5-HT 1A binding was assessed post-mortem using in vitro receptor autoradiography with the agonist [ 3 H]8-OH-DPAT ( 3 H-8-hydroxy-2-[di -n-propylamino]tetralin). Rearing condition did not influence baseline motor impulsivity, but isolation rearing led to decreased baseline cognitive impulsivity. Ethanol did not affect motor impulsivity, but dose-dependently increased impulsive choice in the delay-to-reinforcement task. Enriched rats were more impulsive overall, and isolation-reared rats only showed a shift in impulsive behaviour after 1.2 g/kg. Isolation rearing decreased, and enrichment rearing increased 5-HT 1A binding in the frontal pole of the cortex following experience in the delay-to-reinforcement task. Isolation-reared rats also showed a significant decrease in 5-HT 1A binding in the dentate gyrus of the ventral hippocampus following experience in the delay-to-reinforcement relative to the go/no-go task. These data indicate that differential rearing has a significant influence on cognitive impulsivity, and that altered serotonergic function may underlie these differences.

Adolescent enrichment partially reverses the social isolation syndrome

Early environmental experience produces profound neural and behavioural effects. For example, animals reared in isolation show increased anxiety, neophobia, and poorer performance in learning and spatial memory tasks. We investigated whether later enrichment reverses some or all of the deficits induced by isolation rearing. Eighty-four male Long–Evans rats (21 days old) were reared under different conditions: enriched (group housed with toys), isolated (one rat/cage), standard (two rats/cage), isolated-enriched, enriched-isolated, isolated-standard, or enriched-standard. In the latter four conditions, animals were housed in the first environment until adolescence (66 days). Following the 90-day rearing period, all animals were assessed in a battery of behavioural tests and cortical thickness was measured postmortem. Isolation rearing led to significant differences in behavioural tests measuring anxiety, spatial learning, and locomotor activity; switching the rearing condition partially reversed these changes. Rearing condition did not affect pain thresholds in the tail flick test or aversive associative learning in the conditioned taste aversion test. Enriched rats had the thickest cortex; isolated rats the thinnest. None of the switch groups differed significantly from standard-reared rats in this measure. Taken together, these results provide novel and interesting information regarding the effects of pre- or post-adolescent enrichment experience on behavioural and neural expression of the social isolation syndrome.

Adolescent enrichment partially reverses the social isolation syndrome

Early environmental experience produces profound neural and behavioural effects. For example, animals reared in isolation show increased anxiety, neophobia, and poorer performance in learning and spatial memory tasks. We investigated whether later enrichment reverses some or all of the deficits induced by isolation rearing. Eighty-four male Long–Evans rats (21 days old) were reared under different conditions: enriched (group housed with toys), isolated (one rat/cage), standard (two rats/cage), isolated-enriched, enriched-isolated, isolated-standard, or enriched-standard. In the latter four conditions, animals were housed in the first environment until adolescence (66 days). Following the 90-day rearing period, all animals were assessed in a battery of behavioural tests and cortical thickness was measured postmortem. Isolation rearing led to significant differences in behavioural tests measuring anxiety, spatial learning, and locomotor activity; switching the rearing condition partially reversed these changes. Rearing condition did not affect pain thresholds in the tail flick test or aversive associative learning in the conditioned taste aversion test. Enriched rats had the thickest cortex; isolated rats the thinnest. None of the switch groups differed significantly from standard-reared rats in this measure. Taken together, these results provide novel and interesting information regarding the effects of pre- or post-adolescent enrichment experience on behavioural and neural expression of the social isolation syndrome.

Early Environmental Experience and Transferable Skills in the Weaned Piglet

Early environmental experience can have significant effects on an animal's ability to adapt to challenges in later life. Prior experience of specific situations may facilitate the development of behavioural skills which can be applied in similar situations to later life. In addition, exposure to a more complex environment may enhance cognitive development (eg increased synaptic density), which can then speed the acquisition of new behavioural responses when faced with novel challenges (Grandin 1989).

Experience-dependent changes in the importance of N-methyl- d-aspartate (NMDA) receptors for visual transmission in superior colliculus

The excitatory amino acid transmitter glutamate mediates visual activity in the superficial grey layer (SGS) of superior colliculus. At eye opening N-methyl- d-aspartate receptors (NMDA-rs) convey little of the visual response, but with age their role in visual transmission increases to a peak at P21, then falls to the lower adult level. Visual deprivation which begins before eye opening causes NMDA-rs to assume a greater importance for visual transmission in SGS. Here we explore the possibility that these experience-dependent changes in the role of NMDA-rs in the SGS are limited by age. We find that the effects of visual deprivation on NMDA-r mediated visual activity are recoverable even after extensive dark rearing. Also, a short episode of visual experience is sufficient to allow the normal situation to be established and subsequent dark rearing is ineffective. Four-day periods of visual experience beginning at P14 or P25 have the same effect. Given that NMDA-rs take little part in visual transmission prior to P18, these data prompt a reconsideration of the role of NMDA-r mediated sensory transmission in the mechanisms by which early environmental experience influences the development of the visual system.

Stereotypic Behaviour in Wild Caught and Laboratory Bred Bank Voles (Clethrionymus Glareolus)

AbstractStereotypic behaviour is generally associated with animals maintained in restrictive environments, and has rarely been described in wild or free-ranging animals. The difference between captive and wild populations may be due to their genetic predisposition or to experience of environmental factors. To investigate genetic and environmental factors, we compared the behaviour of 12 wild caught voles and their 9 pups with that of 12 laboratory reared voles and 14 laboratory bred pups. All voles were observed twice. Adults were observed after 10 days housing in a cage, containing food, water, sawdust and hay, and again after 60 days. Pups were observed in the same cages 10 and 60 days after weaning. For each observation, the voles’ behaviour was recorded both undisturbed in this cage, and following introduction to an unfamiliar cage. Locomotor stereotypies were observed in laboratory adults, but not in wild caught voles, which spent less time on all locomotor activities and more time under cover than laboratory voles. There was no difference in mortality or fecundity of laboratory and wild caught voles, so there appeared to be no selective advantage to stereotyping. There was no difference in the behaviour of wild and laboratory pups, so early environmental experience of the cage environment, rather than parental background, was an important factor in the development of locomotor stereotypies in this species. Pups that developed stereotypies by 60 days spent less time under cover and more time walking and climbing after 10 days than voles that did not develop stereotypic behaviour. Stereotypic behaviour may therefore have been derived from persistence of locomotor behaviour. Wild caught voles may have failed to develop locomotor stereotypies, either because they did not perform a locomotor response to captivity or because older voles are less prone to develop novel responses to external cues. It would, therefore, be dangerous to use the absence of stereotypic behaviour as a reliable indicator of welfare without taking into account the animal's prior experience.

Effects of early environmental experience on self-administration of amphetamine and barbital.

Rats were housed after weaning in isolation, with a same-sex sibling, or in a group in an enriched environment for 60 days. Then, subjects were trained to consume all of their fluids during a daily 2-h drinking session, habituated to drinking solutions of both d-amphetamine sulfate and sodium barbital, and then given a choice between drinking water, the stimulant amphetamine and the depressant barbital. Drug choice was affected by both sex and previous housing condition. Males raised in social isolation preferred the stimulant, while females raised in isolation preferred the depressant. Both males and females raised in enriched environments expressed no drug preference, and had the lowest overall drug intake. These results suggest that individual differences in rates of initiation, choice of abusing agent, and maintenance of drug self-administration may be partially determined by pre-existing differences in central nervous system functioning due to early experiences. Differential early experience, particularly the stress of social isolation, can influence drug self-administration behaviour, but the effect may be sex-dependent.

Cerebral lateralization for speech production in congenitally blind adolescents

The effect of early visual deprivation on cerebral lateralization for speech production was investigated using the dual‐task paradigm (tapping with concurrent vocalization). Some 28 right‐handed subjects (14 congenitally blind and 14 normal‐sighted adolescents matched on the basis of sex and age) participated in this study. Results reveal significant suppressions from baseline tapping rates under concurrent vocalization with the right but not the left hand for both groups. These findings suggest that congenital blindness per se does not alter the normal pattern of left hemispheric dominance for speech. The role of adequate early linguistic environmental experience on language lateralization is discussed.

Effect of early environmental experience on the motor development of the preterm infant

A cohort of normally developing preterm infants was subdivided into two gestational age groups (<32 weeks and 32-36 weeks) for the purpose of assessing the impact of the early extrauterine environment on motor development. The motor development of the two groups of infants was assessed and compared at seven points in time: term, 4, 8, and 12 months chronologic age and 4, 8, and 12 months adjusted age. Analyses revealed that certain components of early motor development are biologically driven, whereas other components are affected by the extrauterine environment. The impact of the environment also varied according to the age of the infant. Implications for therapeutic interventions for infants with motor disorders are discussed.