Sensitive Period For Learning Research Articles

Wanting to matter and learning to care: A neurodevelopmental window of opportunity for (Pro) social learning?

Wanting to matter—to feel socially recognized, appreciated, and capable of actions that benefit others—represents a fundamental motivation in human development. The motivational salience of mattering appears to increase in adolescence. Evidence suggests this is related to pubertal increases in the incentive salience for gaining social value and personal agency. This can provide a useful heuristic for understanding motivational proclivities (i.e. wanting to matter) that influence action-outcome learning as young adolescents are exploring and learning how to navigate increasingly complex social and relational environments. Adolescence also brings new capacities, motives, and opportunities for learning to care about and contribute to the benefit of others. Together, these create a window of opportunity: a sensitive period for learning to gain salient feelings of mattering through caring prosocial actions and valued societal contributions. Successfully discovering ways of mattering by doing things that matter to others may contribute to formative socio-emotional learning about self/other. Advances in understanding these social and relational learning processes and their neurodevelopmental underpinnings can inform strategies to improve developmental trajectories of social competence and wellbeing among adolescents growing up in a rapidly changing and increasingly techno-centric world.

Appropriate knowledge of wild chimpanzee behavior (‘know-what’) and field experimental protocols (‘know-how’) are essential prerequisites for testing the origins and spread of technological behavior. Response to “Unmotivated subjects cannot provide interpretable data and tasks with sensitive learning periods require appropriately aged subjects” by C. Tennie and J. Call

We respond to the commentary by Tennie and Call (2023) on the article by Koops et al. (2022) in Nature Human Behaviour titled ‘Field experiments find no evidence that chimpanzee nut cracking can be independently innovated.’ Koops et al. (2022) showed that chimpanzee nut cracking is not a so-called ‘latent solution.’ Chimpanzees (Pan troglodytes verus) in the Nimba Mountains (Guinea) did not crack nuts when presented with nuts and stones in ecologically valid field experiments. In their Commentary, Tennie and Call (2023) argued that the experiments were inconclusive for two reasons: 1) the chimpanzees were not motivated to treat the nuts as food, and 2) the chimpanzees were not within the appropriate ‘sensitive learning period.’ In our response, we argue that Tennie and Call (2023) incorrectly use the term ‘motivation’ to mean ‘willingness to eat the nut’, which requires existing knowledge of the edibility of the nuts. We also point out that it is unnatural and uninformative to inject nuts with honey to motivate the chimpanzees to eat them, as suggested by Tennie and Call (2023). Finally, we highlight that Koops et al. (2022) tested appropriately aged subjects (N=32 immatures). Moreover, we argue that there is no evidence to suggest that there is a strictly sensitive learning period restricted to juvenility. Finally, we emphasize the need for researchers doing experiments in captivity to visit their study species in the wild, and for field researchers to be involved in efforts to design ecologically valid experiments in captivity.

Handwriting kinematics during learning to write with the dominant left hand in converted left-handers

Converting left-handers to their non-dominant right hand was previously widespread, particularly for handwriting. The present study aimed to explore the extent to which adult, converted left-handers can learn writing with their dominant left hand during a 2-year training program. Eleven converted left-handers participated in the training. Handwriting kinematics were assessed at regular intervals (seven sessions) and compared to those of 11 innate left-handed controls matched for age, gender, and overall handedness score for basic (Finger, Wrist, Circle) and complex (Sentence, Copy) handwriting tasks. Regarding basic tasks in the training group, we found rapid increases in left and right-hand frequency and no significant differences between both hands at any time point, indicating successful hand transfer. After 24 months, training participants significantly surpassed controls for writing frequency in basic tasks with their left hand. For complex tasks, we identified significant increases in the training groups’ left-hand writing frequency and duration between the first and last session. While training participants’ left-hand writing remained significantly slower than their right-hand writing, statistics confirmed final differences between hands only for the duration of the Sentence task. Importantly, left-hand writing in the training group was characterized by lower frequency, lower automaticity, and prolonged duration after 24 months compared to innate left-handers. With training participants’ left-hand writing skills significantly increasing for complex tasks and no final statistically significant differences between hands for frequency and automaticity, the program was considered effective. Nevertheless, within 2 years, training participants did not reach innate left-handers handwriting proficiency for complex tasks. Underlying reasons may be various, such as a non-optimal training program, a sensitive period for learning to write, irreversible neural changes during conversion in childhood, age-related decline of motor learning capacity, or retrograde interference between right- and left-hand writing.

Connecting inside out: Development of the social brain in infants and toddlers with a focus on myelination as a marker of brain maturation.

Early childhood is a sensitive period for learning and social skill development. The maturation of cerebral regions underlying social processing lays the foundation for later social‐emotional competence. This study explored myelin changes in social brain regions and their association with changes in parent‐rated social‐emotional development in a cohort of 129 children (64 females, 0–36 months, 77 White). Results reveal a steep increase in myelination throughout the social brain in the first 3 years of life that is significantly associated with social‐emotional development scores. These findings add knowledge to the emerging picture of social brain development by describing neural underpinnings of human social behavior. They can contribute to identifying age‐/stage‐appropriate early life factors in this developmental domain.

Testing the individual and social learning abilities of task-naïve captive chimpanzees (Pan troglodytes sp.) in a nut-cracking task.

Nut-cracking is often cited as one of the most complex behaviours observed in wild chimpanzees. However, the cognitive mechanisms behind its acquisition are still debated. The current null hypothesis is that the form of nut-cracking behaviour relies on variants of social learning, with some researchers arguing, more precisely, that copying variants of social learning mechanisms are necessary. However, to date, very few experiments have directly investigated the potentially sufficient role of individual learning in explaining the behavioural form of nut-cracking. Despite this, the available data provides some evidence for the spontaneous acquisition of nut-cracking by chimpanzees; later group acquisition was then found to be at least facilitated by (unspecified) variants of social learning. The latter findings are in line with both suggested hypotheses, i.e., that copying social learning is required and that other (non-copying) social learning mechanisms are at play. Here we present the first study which focused (initially) on the role of individual learning for the acquisition of the nut-cracking behavioural form in chimpanzees. We tested task-naïve chimpanzees (N = 13) with an extended baseline condition to examine whether the behaviour would emerge spontaneously. After the baseline condition (which was unsuccessful), we tested for the role of social learning by providing social information in a step-wise fashion, culminating in a full action demonstration of nut-cracking by a human demonstrator (this last condition made it possible for the observers to copy all actions underlying the behaviour). Despite the opportunities to individually and/or socially learn nut-cracking, none of the chimpanzees tested here cracked nuts using tools in any of the conditions in our study; thus, providing no conclusive evidence for either competing hypothesis. We conclude that this failure was the product of an interplay of factors, including behavioural conservatism and the existence of a potential sensitive learning period for nut-cracking in chimpanzees. The possibility remains that nut-cracking is a behaviour that chimpanzees can individually learn. However, this behaviour might only be acquired when chimpanzees are still inside their sensitive learning period, and when ecological and developmental conditions allow for it. The possibility remains that nut-cracking is an example of a culture dependent trait in non-human great apes. Recommendations for future research projects to address this question are considered.

Behavioural outcomes of housing for domestic dog puppies (Canis lupus familiaris)

Domestic dogs experience a sensitive period for learning during early life and conditions during this time can have important consequences in the adult. We investigated the effects of kennel environment during early life, comparing the temperaments of puppies reared in indoor kennels, located in the breeder’s house, with those reared in outdoor kennels, located outside the breeder’s house and with limited human contact. The study was conducted on 264 puppies from 44 litters belonging to 21 breeds. Of these, 160 puppies were reared in indoor kennels (70 female and 90 male puppies, 27 litters) and 104 in outdoor kennels (52 female and 52 male, 17 litters). We conducted PAT (Puppy Aptitude Testing) tests to measure puppy temperament at an age of seven or eight weeks. Using a gamma GLMM fitted using Bayesian inference, we showed a statistically important effect of kennelling on posterior mean PAT scores. Puppies kennelled outdoors scored higher on PAT testing, irrespective of sex or age, and after accommodating for dependency in the data due to litter identity. Puppies raised outdoors showed an elevated tendency for submissive behaviour, a greater risk of aggression through fear, and a lowered capacity for coping with novel conditions. These findings have direct implications for dog breeders and illustrates that enrichment of the environment of dam and puppies can mitigate the risk of behavioural problems in adult dogs.

Early social experience alters transcriptomic responses to species-specific song stimuli in female songbirds

Amongst an array of stimuli from countless species, animals must recognize salient signals, including those of their own species. In songbirds, behavioral tests have demonstrated that preferences for conspecific male songs are determined by both preexisting biases and social experience with a male ‘tutor’ during the sensitive period for learning. Although immediate early gene expression (e.g. ZENK) and electrophysiological experiments generally find greater neural responses for conspecific songs, it remains unclear whether distinct mechanisms, such as sensory gating, are engaged to filter out irrelevant heterospecific songs. Here we compare the transcriptomic profiles, via RNA-seq, of non-singing females of a songbird, the zebra finch (Taeniopygia guttata), by focusing on the auditory forebrain, a region known to be critical in the processing of conspecific vs. heterospecific songs. Gene expression profiles demonstrate that different neural mechanisms are involved in the processing of conspecific versus heterospecific Bengalese finch (Lonchura striata) songs. In particular, one gene known to mediate sensory gating, the alpha 3 subunit member of nicotinic cholinergic receptors (CHRNA3), was significantly downregulated in response to hearing Bengalese finch song, but not when young females were tutored by a Bengalese male during early development. Overall, our results confirm previous behavioral and physiological studies, such that heterospecific-tutored individuals processed both conspecific and tutor songs similarly. Using transcriptomic profiling of peripheral blood samples, we also demonstrate the methodological potential of non-terminal sampling to identify transcriptomic biomarkers for conspecific auditory recognition. These results show how experience and inherited preferences facilitate the neural processing of salient songs by female songbirds.

9.2 Caregiver Presence Modifies Neural Networks Processing of Trauma in Infancy

A sensitive period for learning about the attachment figure typifies the early life of altricial species, such as humans and rodents.

On the impact of L2 speech rhythm on syntactic ambiguity resolution

In an event-related potential (ERP) study we investigated the role of age of acquisition (AoA) on the use of second language rhythmic properties during syntactic ambiguity resolution. Syntactically ambiguous sentences embedded in rhythmically regular and irregular contexts were presented to Turkish early and late second language (L2) learners of German and to German monolingual controls. Regarding rhythmic properties, Turkish is syllable-timed and prefers the iamb as its metric foot, while German is stress-timed, relying on the trochee. To utilize rhythm during the processing of syntactic ambiguity in L2, Turkish early and late L2 learners of German must master different rhythmic properties than in their first language. ERPs reveal a reduction in the P600 response to object-first sentences presented in rhythmically regular, but not in rhythmically irregular contexts for early learners and monolinguals only. No such effect was found for late L2 learners. Results indicate an interactive use of rhythmic information during the processing of syntactic ambiguity by monolinguals and early learners. Further, data from late L2 learners suggest that the acquisition of rhythmic properties may have to occur in a sensitive learning period.

Auditory experience refines cortico-basal ganglia inputs to motor cortex via remapping of single axons during vocal learning in zebra finches

Experience-dependent changes in neural connectivity underlie developmental learning and result in life-long changes in behavior. In songbirds axons from the cortical region LMAN(core) (core region of lateral magnocellular nucleus of anterior nidopallium) convey the output of a basal ganglia circuit necessary for song learning to vocal motor cortex [robust nucleus of the arcopallium (RA)]. This axonal projection undergoes remodeling during the sensitive period for learning to achieve topographic organization. To examine how auditory experience instructs the development of connectivity in this pathway, we compared the morphology of individual LMAN(core)→RA axon arbors in normal juvenile songbirds to those raised in white noise. The spatial extent of axon arbors decreased during the first week of vocal learning, even in the absence of normal auditory experience. During the second week of vocal learning axon arbors of normal birds showed a loss of branches and varicosities; in contrast, experience-deprived birds showed no reduction in branches or varicosities and maintained some arbors in the wrong topographic location. Thus both experience-independent and experience-dependent processes are necessary to establish topographic organization in juvenile birds, which may allow birds to modify their vocal output in a directed manner and match their vocalizations to a tutor song. Many LMAN(core) axons of juvenile birds, but not adults, extended branches into dorsal arcopallium (Ad), a region adjacent to RA that is part of a parallel basal ganglia pathway also necessary for vocal learning. This transient projection provides a point of integration between the two basal ganglia pathways, suggesting that these branches convey corollary discharge signals as birds are actively engaged in learning.

Defining age limits of the sensitive period for attachment learning in rat pups.

Enhanced odor preference learning and attenuated fear learning characterizes rat pups' attachment learning Sensitive Period for learning the maternal odor. This period terminates at 10 days old (PN10) with increasing endogenous levels of the stress hormone, corticosterone. Increasing Sensitive Period pups' corticosterone prematurely terminates the Sensitive Period, while decreasing corticosterone in older pups delays Sensitive Period termination. Here we extend these findings and define the age range corticosterone alters learning and question whether corticosterone permanently terminates the Sensitive Period. Pups were odor-0.5 mA shock conditioned with either corticosterone increased (PN5-6; 4 mg/kg vs. saline) or decreased (PN15-16; naturally by maternal presence or corticosterone synthesis blocker, Metyrapone). Finally, PN7-8 pups were conditioned with corticosterone and reconditioned without corticosterone to assess whether the Sensitive Period was permanently terminated. Results indicate developmental limits for corticosterone regulation of pup learning are PN6 through PN15. Furthermore, inducing precocious corticosterone induced fear learning was not permanent, since reconditioning without corticosterone enabled odor preference learning. Results suggest pups are protected from learning aversions to maternal odor until approaching weaning.

Bird song learning as an adaptive strategy.

Parallels are often drawn between bird song learning and human language learning. The analogies include an early sensitive period for learning, separation of sensory and motor phases of learning, 'innate knowledge' of language or song, and specialized neural systems. Nevertheless, in distinction to human language learning, song learning is usually viewed as a purely auditory process. This view is implied in the typical experimental paradigm for studying song learning, in which the bird is isolated in a sound-proof chamber and exposed only to tape-recorded song. This paradigm remains the major method of studying song learning despite recent demonstrations of the importance of social variables, and it contains the implicit assumption that non-auditory variables, especially social and ecological variables, play only a minor role in this process. I will argue here that understanding the functions of song learning requires that we investigate it in the field, where social and ecological variables have full play. We have done just this for the song sparrow, and when viewed in this perspective song learning in the song sparrow takes on the clear outlines of an adaptive strategy.

Étude de l'agressivité physique chez le jeune enfant : comparaison d'une population française et d'une population canadienne

Studies of aggression often confound physical aggression with verbal aggression, indirect aggression, opposition, competition and other externalizing behaviours. Yet little is known about the onset and development of physical aggression before school entry. Recently, Tremblay et al. [27] have interested in this field study. In a transcultural perspective, we have tried to replicate, using the same method, the results they obtained. It appears that the data we have collected concord with Tremblay’s data: the maternal reports on 11 physically aggressive behaviours indicated that the rate of cumulative onset of physically aggressive behaviours increased substantially from 12 to 17 months after birth. By 17 months of age, onset of physical aggression is reported for close 90% of the children. Moreover, the sex of the child and the presence of a sibling appeared to influence age of onset. Both studies suggest that the notion of increased probability of onset of physical aggression as children approach adolescence needs to be reconsidered. Most children have had their onset of physical aggression by the end of their second year after birth, and most have learn to inhibit physical aggression by school entry. Thus, there may be two main developmental trajectories of physical aggression: childhood limited and life-course persistent. This may be an indication that there is a sensitive period for learning to inhibit physically aggressive behaviour.

Unique characteristics of neonatal classical conditioning: The role of the amygdala and locus coeruleus

The central nervous system of altricial infants is specialized for optimizing attachments to their caregiver. During the first postnatal days, infant rats show a sensitive period for learning and are particularly susceptible to learning an attraction to their mother's odor. Classical conditioning appears to underlie this learning that is expressed behaviorally as an increased ability to acquire odor preferences and a decreased ability to acquire odor aversions. Specifically, in neonatal rats, pairing an odor with moderately painful shock (0.5mA) or milk produces a subsequent relative preference for that odor. The neural circuitry supporting the increased ability to acquire odor preferences appears to be the heightened functioning of the noradrenergic pontine nucleus locus coeruleus. Indeed, norepinephrine from the locus coeruleus appears to be both necessary and sufficient for learning during the sensitive period. On the other hand, the decreased ability to acquire odor aversions seems to be due to the lack of participation of the amygdala in at least some aversive learning situations. The site of plasticity in the pup's brain appears to be limited to the olfactory bulb. This neonatal sensitive period for learning ends around postnatal day 9-10, at which time pups make the transition from crawling to walking and classical conditioning becomes "adultlike." The neonatal behavioral and neural induced changes are retained into adulthood where it modifies sexual behavior.

The ontogeny of the homing pigeon navigational map: evidence for a sensitive learning period.

Homing pigeons can learn a navigational map by relying on the heterogeneous distribution of atmospheric odours in the environment. To test whether there might be a sensitive period for learning an olfactory-based navigational map, we maintained a group of young pigeons in an aviary screened from the winds until the age of three to four months post-fledging. Subsequently, the screens were removed and the pigeons were exposed to the winds and the environmental odours they carry for three months. One control group of pigeons was held in a similar aviary but exposed to the winds immediately upon Hedging, while another control group of pigeons was allowed free-flight. When the pigeons from the three groups were released from two distant release sites at about six months of age post-fledging, the two control groups were found to be equally good at orientating and returning home, while the experimental pigeons held in the shielded aviary for the first three months post-fledging were unable to orientate homeward and they were generally unsuccessful in returning home. This result supports the hypothesis that environmental experience during the first three months post-fledging is critical for some aspect of navigational map learning and that navigational map learning displays sensitive period-like properties.

The search for the age of ‘onset’ of physical aggression: Rousseau and Bandura revisited

AbstractBackgroundStudies of aggression often confound physical aggression with verbal aggression, indirect aggression, relational aggression, opposition, competition and other externalizing behaviours. Developmental models of aggression have suggested that onset of physical aggression occurs after the onset of hyperactive, stubborn and oppositional behaviour. Yet little is known about the onset and development of physical aggression before school entry.MethodThe age of onset and frequency of physical aggression was studied in a population sample of 17‐month‐old children.ResultsThe 511 maternal reports on 11 physically aggressive behaviours indicated that the rate of cumulative onset of physically aggressive behaviours increased substantially from 12 to 17 months after birth. By 17 months of age, onset of physical aggression was reported for close to 80% of the children. However, the sex of the child and the presence of a sibling appeared to influence age of onset.ConclusionsThese results, and those of other studies of preschool children, suggest that the notion of increased probability of ‘onset’ of physical aggression as children approach adolescence needs to be reconsidered. Most children have had their ‘onset’ of physical aggression by the end of their second year after birth, and most have learned to inhibit physical aggression by school entry. Thus, there may be two main developmental trajectories of physical aggression: childhood limited, and life‐course persistent. This may be an indication that there is a sensitive period for learning to inhibit physically aggressive behaviour. To understand and prevent cases of chronic physical aggression, which appear most at risk of violent criminal behaviour, we need to study the factors which help children learn to inhibit physical aggression during the preschool years. Copyright © 1999 Whurr Publishers Ltd.

Adaptiveness of food learning and food aversions in children

This paper uses an evolutionary perspective to explain features of food learning in human children. Data from Western parents indicate that (1) children are least picky about foods when they are between one and two years of age, (2) vegetables are frequently refused by children, and (3) children have a tendency to eat foods one at a time rather than mixed together. Adaptive explanations for these patterns are suggested, together with supporting evidence from studies of the ontogeny of human and non-human primate diet choice. The following arguments are made: (1) age difference in receptiveness to new foods is consistent with the existence of a sensitive period for learning about food; (2) since leaves and other non-fruit plant parts often contain toxic secondary compounds and young animals are less able to detoxify these chemicals than are adults, an initial dislike of vegetables may function to protect young children against the risk of poisoning; (3) a preference for easily identifiable foods eaten separately may be an evolved preference that aids in identification of the food and the consequences of eating it.

Developmental changes in carbachol-stimulated phosphoinositide turnover in synaptoneurosomes of the robust nucleus of the archistriatum in the zebra finch.

The effects of acetylcholine (ACh) on synaptoneurosomes of the robust nucleus of the archistriatum (RA), one of the song control nuclei, were investigated during the sensitive period of song learning in the zebra finch. Carbachol (an ACh agonist) stimulated phosphoinositide (PI) turnover at three different ages. Corresponding to a marked increase in ACh levels in the RA, carbachol-stimulated PI turnover peaked during the most sensitive learning period in the life of the zebra finch. These findings suggest that ACh contributes to the regulation of synaptic plasticity in RA neurones involved with song learning in the zebra finch.

A sensitive period for learning about food

It is proposed here that there is a sensitive period in the first two to three years of life during which humans acquire a basic knowledge of what foods are safe to eat. In support of this, it is shown that willingness to eat a wide variety of foods is greatest between the ages of one and two years, and then declines to low levels by age four. These data also show that children who are introduced to solids unusually late have a narrower diet breadth throughout childhood, perhaps because the duration of the sensitive period has been shortened. By reducing the costs associated with learning, a sensitive period for food learning should be adaptive for any omnivore (including early humans) that remains in the same environment throughout its life.

Projection neurons within a vocal motor pathway are born during song learning in zebra finches.

Many birds learn song during a restricted 'sensitive' period. Juveniles memorize a song model, and then learn the pattern of muscle contractions necessary to reproduce the song. Of the neural changes accompanying avian song learning, perhaps the most remarkable is the production of new neurons which are inserted into the hyperstriatum ventralis pars caudalis (HVc), a region critical for song production. We report here that in young male zebra finches many of the new neurons incorporated into the HVc innervate the robust nucleus of the archistriatum (RA) which projects to motor neurons controlling the vocal musculature. Furthermore, far fewer of these new neurons are incorporated into the HVc of either adult males that are beyond the sensitive learning period, or young females (who do not develop song). Thus, a major portion of the vocal motor pathway is actually created during song learning. This may enable early sensory experience and vocal practice to not only modify existing neuronal circuits, but also shape the insertion and initial synaptic contacts of neurons controlling adult song.