In this longitudinal study it was observed that: (1) fear conditioning increases with age, (2) somewhat different growth curves were observed for the three different conditioned fear response components, (3) for conditioning overall and all three conditioning components, there was a noticeable increase from ages 5 to 6, (4) individual differences in arousal, orienting, and UCR correlated with individual differences in conditioning at each age, with a substantial increase in the influence of these three processes from ages 5 to 6. Findings constitute the first developmental study of SC fear conditioning in early childhood, and suggest that complex automatic and controlled cognitive / emotional processes are involved in SC conditioning that increases across ages in early childhood.
A key finding of this study was the age-related changes in conditioning. As expected, conditioning significantly increased with age (see ). Though it has widely been accepted that human autonomic conditioning could be fully accounted for in terms of expectancy (e.g., Dawson, 1973
; Dawson & Schell, 1987
), some studies have suggested that a different process is involved in addition to orienting and conscious conditioning processes. For example, Schell et al. (1991)
reported that even though subjects no longer expected the UCS after the CS+ based on their self-reports, they nevertheless continued showing reliable differential responding between the CS+ and the CS−. Several studies have argued that conscious awareness of contingency is not a necessary component for conditioning to occur and instead have proposed a two-level learning model involving automatic / emotional, and also conscious / cognitive processes (Bridger & Mandel, 1964
; Mandel & Bridger, 1973
). In this two-level model, one cognitive level involves the consciously learned CS-UCS association, which then results in the modification of responses related to orienting (Dawson & Schell, 1987
; Öhman, 1974
; Siddle, 1991
). Another more automatic / emotional level involves the acquisition of conditioned defensive responses to an aversive CS, and this process does not require conscious awareness of the CS-UCS contingency and may reflect modification of a primitive fear network involving amygdala and the right cerebral hemisphere (Hodes, Cook, & Lang, 1985
; Hugdahl, 1995
). Consequently the increase in conditioning with age is likely to reflect not just an increase in basic (automated) attentional processes, but also increased conscious, controlled cognitive processes related to conscious contingency awareness.
One of the surprising findings was that conditioning was observed as early as age 3, despite the facts that (i) the UCS was not particularly intense (90 dB), (ii) a partial reinforcement schedule was used, (iii) the difference between the CS+ and CS− involved only a modest frequency change of 500 Hz, and (iv) a short number of conditioning trials were used. These combined conditions would be anticipated to make it relatively difficult to observe conditioning in young children, and yet evidence for significant conditioning was nevertheless observed. The implication for future developmental studies is that researchers can employ only modestly aversive and temporally short (7.5 minutes) paradigms to obtain a measure of fear conditioning in children, with minimal risk from a human subjects perspective. The belief that this is not entirely possible with young children may have deterred developmental researchers from implementing fear conditioning paradigms with vulnerable child populations. Finally, although ANOVA results suggested that SC conditioning emerges no earlier than age 8 years, latent growth curve modeling demonstrated that children show conditioning as early as age 3 years. This discrepancy may possibly be due to the listwise deletion used in ANOVA, whereas the EM algorithm used in latent growth curve modeling is considered to lead to less biased estimation and more reliable results.
The different components of SC conditioning showed somewhat different growth patterns across age, with more erratic and complex development of the first and third interval response at early ages compared to the relatively more linear development of the second interval response. In attempting some initial understanding of these differences, the first and third interval response are thought to reflect conditioned orienting responses, whereas the second interval response is thought to reflect a partially separate expectancy or preparatory learning process (Öhman, 1979
). In an fMRI study measuring SC responses to fear stimuli, Williams et al. (2000)
found that fear stimuli which elicit an SC response were associated with activation of the amygdala and medial frontal cortex, whereas fear stimuli which did not evoke SC responses activated a hippocampal-lateral network. They argued that while the amygdala-medial frontal network was preferentially involved in the visceral experience of threat, the hippocampal-lateral frontal network reflected activation of declarative and contextual processing of threatening stimuli. First and third interval response may therefore more reflect amygdala-medial frontal automated processing while the second interval response may reflect more controlled hippocampal-lateral prefrontal activation.
Although conditioning generally increased with age for the second interval response (see ), this was not true for the first interval response. In particular, conditioning of the first interval response was unexpectedly higher
at age 3 than at age 4 (see ). One possible explanation for this finding is that the first test session was particularly stressful for the young children, which may also partly contribute to the large variance of the assessment at age 3 (see ). Anecdotal reports from adult participants of this longitudinal study to research staff and reported to one of the authors (AR) indicate that they particularly remembered testing in the small cubicle at age 3 where conditioning took place, and that this was generally a stressful experience. Animal and human research has shown that stress facilitates the development of classical conditioning (Cordero, Venero, Kruyt, & Sandi, 2003
; Jackson, Payne, Nadel, & Jacobs, 2006
). In contrast, during testing the following year at age 4, some habituation to the stress of the laboratory testing would be anticipated, resulting in a reduction in conditioning (first interval response – see ). Alternatively, the child sat on the mother's lap at age 3 years, but not thereafter, and this may have facilitated arousal, which in turn, facilitated conditioning. It is noted, however, that this stress / arousal explanation cannot be applied adequately to the third interval response, which increased
from 3 to 4 years.
The findings of different developmental trajectories for the first and second interval response in the current study are consistent with previous studies showing dissociation of these two components. For example, Backs and Grings (1985)
recorded first and second interval responses in a long ISI conditioning paradigm and found that only the first interval response increased as a function of the objective probability of UCS occurrence, indicating preparation for the impending aversive event. Cheng et al. (2007)
used fMRI and concurrent SC measurements and found that the first interval response is associated with activation
of the amygdala, while the second interval response is associated with deactivation
of amygdala. In addition, the deactivation of amygdala during the second interval response has been argued to represent strategies that attenuate responsiveness to the aversive UCR (Cheng et al., 2007
; Petrovic et al., 2004
). Similarly, Hare argued that psychopaths give a larger-than-normal cardiovascular anticipatory fear response that attenuates the responsiveness of the UCR (Hare, 1978
). It is worth noting that in the current study ANOVA results have suggested that the second interval response, relative to the first and the third interval response, may show later development (at age 8). Therefore, the second interval response may be an autonomic indicator of the capacity to cope with stress, and the later development of this component may suggest that this emotion regulation capability requires more resources and emerges relatively later in children. Future developmental studies measuring both first and second interval responses and emotion regulation could further test the prediction that the second interval response is more related to emotion-regulation.
For conditioning in general, it can be seen from that conditioning showed a marked increase from ages 5 to 6 years. Indeed, inspection of indicates that this increase was the most consistent part of the growth curve across the three conditioning components. The increase in conditioning from ages 5 to 6 years is partly consistent with findings documenting the growth of the cerebral hemispheres across the first ten years of life, with a very pronounced increment in electroencephalographic (EEG) phase present in left temporal-frontal electrode sites from age 4 to 6 years (Thatcher, Walker, & Giudice, 1987
) and the highest level of rate of EEG coherence growth between frontal and posterior lobes at age 6 (Thatcher, 1992
). It is worth noting that SC orienting was also found to show a pronounced increase from ages 5 to 6 in this same sample (Gao et al., 2007
). In the current sample, at age 5 years children began to enter state schools. This environmental change may constitute a mild stressor which could facilitate fear conditioning at this age. In addition, given that environmental enrichment in animals has been shown to result in neurogenesis in the hippocampus (Kempermann & Gage, 1999
), and given the role of the hippocampus in both fear conditioning (Bast et al., 2003
; Knight et al., 2004
) and orienting (Critchley, 2002
; Williams et al., 2000
), the novelty of the school experience at age 5-6 may partly explain why association learning markedly increased at this age. Conceivably, neurogenesis in the hippocampus caused by novelty and environmental enrichment may contribute to both the periods of major change in EEG coherence, orienting, and conditioning at this age period.
A subsidiary question of this study concerned what psychophysiological factors are associated with fear conditionability within each age group. The availability of pre-conditioning measures of arousal, orienting, and UCR data at four of the five ages allowed us to examine the extent to which these processes are correlated with conditioning. Results demonstrated that all three processes are positively associated with individual differences in conditioning. The amount of variability they explained in conditionability increased from 17.2% at age 3 to 28.8% at age 6 (). While it cannot be concluded that higher orienting, arousal, and UCR are causally associated with better conditioning, the fact that all three measures precede the onset of the first conditioned response in this experiment rules out the possibility that higher fear conditioning causes increases in the three processes. It is instead conceivable that higher arousal, orienting and UCR partly facilitate better conditioning. For example, because two of the three conditioned responses (first and third interval response) are known to have a significant orienting component, increased orienting could reasonably be expected to facilitate better conditioning. Furthermore, children who give a larger UCR may be expected to be more fearful of the UCS; because a more aversive UCS is known to give rise to stronger fear conditioning (Prokasy & Kumpfer, 1973
) children who are more responsive to the UCS may be expected to show a stronger UCR. Alternatively, third factors (e.g., individual differences in brain processes that regulate arousal and information- processing) may result in across-the-board increases in all processes.
One further developmental finding is that stepwise linear regression showed that while SC level (at age 3) and UCR (at age 4) had significant influences at these early ages, their influence decreased over time and was replaced by the strong influence of orienting whose contribution to conditioning increased from explaining 3.2% of the variance at age 3 to 25.4% at age 6 (see ). This may be due to the developmental increase in orienting previously observed in this sample (Gao et al., 2007
). Indeed, the developmental profiles of orienting (Gao et al., 2007
) and conditioning are strikingly similar. This may be partly due to the fact that two of the three components of conditioning (first and third interval response) are orienting in nature, reflecting the potential importance of orienting in the facilitation of conditioning.
Experimental research attempting to understand the development of fear conditioning in children has clinical neuroscience and developmental neuroscience implications. As mentioned above, Rich et al. (2006)
have argued that a paradigm shift is occurring in clinical neuroscience whereby psychiatric illnesses are increasingly being viewed as neurodevelopmental in nature, and that assessment of amygdala dysfunction can help elucidate the neurodevelopmental basis of bipolar disorder in children. Similarly, Pine et al. (2001)
have argued strongly that fMRI paradigms should be developed to assess amygdala functioning in children, and that there is a critical need for the assessment of fear conditioning in childhood as a risk factor for anxiety disorders in adulthood. In this context, understanding the development of the amygdala-related processes such as the conditioned fear response in children may be critically important in understanding the etiology of adolescent and adult clinical conditions. Until functional imaging studies are able to more easily scan young children in the 3-8 year age range, a relative strength of the SC fear conditioning paradigm for child development researchers is that it allows for an indirect assessment of the neural networks subserving different forms of information-processing, in particular, the specific circuit generally implicated in fear conditioning which centrally involves the amygdala.
In conclusion, this experimental longitudinal study documents a relatively linear increase in SC fear conditioning in early childhood from ages 3 to 8 years, suggesting a gradual development of a complex automatic and controlled cognitive / emotional process in early childhood. While the more controlled expectancy and preparatory processes reflected in the second interval response develop relatively late, the stress of first testing could have produced the accentuated conditioning observed in the more orienting-related first interval response. The marked increase in average conditioning from 5 to 6 years may be accounted for by the increasing roles of arousal, orienting, and the UCR at this time (see ) and the stress and novelty / environmental enrichment associated with transition from home to formal state schools at this age. The utilization of the SC fear conditioning paradigm may provide probably the best (albeit indirect) proxy measure of amygdala functioning which can be quickly and easily assessed in young community children below functional brain scanning age.