Helena J. V. Rutherford

Thriving and Surviving: Approach and Avoidance Motivation and Lateralization

Two core motivational systems have been conceptualized as underlying emotion and behavior. The approach system drives the organism toward stimuli or events in the environment, and the avoidance system instead deters the organism away from these stimuli or events. This approach—avoidance dichotomy has been central to theories of emotion. Advances in neuroscience complementing well-designed behavioral experiments have begun to elucidate the neural mechanisms underlying approach—avoidance motivation, suggesting that these two systems exist in parallel and are lateralized in the brain. This review explores the notion of approach—avoidance and the cerebral lateralization of these motivational tendencies.

Maternal neural responses to infant cries and faces: relationships with substance use

Substance abuse in pregnant and recently post-partum women is a major public health concern because of effects on the infant and on the ability of the adult to care for the infant. In addition to the negative health effects of teratogenic substances on fetal development, substance use can contribute to difficulties associated with the social and behavioral aspects of parenting. Neural circuits associated with parenting behavior overlap with circuits involved in addiction (e.g., frontal, striatal, and limbic systems) and thus may be co-opted for the craving/reward cycle associated with substance use and abuse and be less available for parenting. The current study investigates the degree to which neural circuits associated with parenting are disrupted in mothers who are substance-using. Specifically, we used functional magnetic resonance imaging to examine the neural response to emotional infant cues (faces and cries) in substance-using compared to non-using mothers. In response to both faces (of varying emotional valence) and cries (of varying distress levels), substance-using mothers evidenced reduced neural activation in regions that have been previously implicated in reward and motivation as well as regions involved in cognitive control. Specifically, in response to faces, substance users showed reduced activation in prefrontal regions, including the dorsolateral and ventromedial prefrontal cortices, as well as visual processing (occipital lobes) and limbic regions (parahippocampus and amygdala). Similarly, in response to infant cries, substance-using mothers showed reduced activation relative to non-using mothers in prefrontal regions, auditory sensory processing regions, insula and limbic regions (parahippocampus and amygdala). These findings suggest that infant stimuli may be less salient for substance-using mothers, and such reduced saliency may impair developing infant-caregiver attachment and the ability of mothers to respond appropriately to their infants.Substance abuse in pregnant and recently post-partum women is a major public health concern because of effects on the infant and on the ability of the adult to care for the infant. In addition to the negative health effects of teratogenic substances on fetal development, substance use can contribute to difficulties associated with the social and behavioral aspects of parenting. Neural circuits associated with parenting behavior overlap with circuits involved in addiction (e.g., frontal, striatal, and limbic systems) and thus may be co-opted for the craving/reward cycle associated with substance use and abuse and be less available for parenting. The current study investigates the degree to which neural circuits associated with parenting are disrupted in mothers who are substance-using. Specifically, we used functional magnetic resonance imaging to examine the neural response to emotional infant cues (faces and cries) in substance-using compared to non-using mothers. In response to both faces (of varying emotional valence) and cries (of varying distress levels), substance-using mothers evidenced reduced neural activation in regions that have been previously implicated in reward and motivation as well as regions involved in cognitive control. Specifically, in response to faces, substance users showed reduced activation in prefrontal regions, including the dorsolateral and ventromedial prefrontal cortices, as well as visual processing (occipital lobes) and limbic regions (parahippocampus and amygdala). Similarly, in response to infant cries, substance-using mothers showed reduced activation relative to non-using mothers in prefrontal regions, auditory sensory processing regions, insula and limbic regions (parahippocampus and amygdala). These findings suggest that infant stimuli may be less salient for substance-using mothers, and such reduced saliency may impair developing infant-caregiver attachment and the ability of mothers to respond appropriately to their infants.

Disruption of Maternal Parenting Circuitry by Addictive Process: Rewiring of Reward and Stress Systems

Addiction represents a complex interaction between the reward and stress neural circuits, with increasing drug use reflecting a shift from positive reinforcement to negative reinforcement mechanisms in sustaining drug dependence. Preclinical studies have indicated the involvement of regions within the extended amygdala as subserving this transition, especially under stressful conditions. In the addictive situation, the reward system serves to maintain habitual behaviors that are associated with the relief of negative affect, at the cost of attenuating the salience of other rewards. Therefore, addiction reflects the dysregulation between core reward systems, including the prefrontal cortex (PFC), ventral tegmental area (VTA), and nucleus accumbens (NAc), as well as the hypothalamic–pituitary–adrenal axis and extended amygdala of the stress system. Here, we consider the consequences of changes in neural function during or following addiction on parenting, an inherently rewarding process that may be disrupted by addiction. Specifically, we outline the preclinical and human studies that support the dysregulation of reward and stress systems by addiction and the contribution of these systems to parenting. Increasing evidence suggests an important role for the hypothalamus, PFC, VTA, and NAc in parenting, with these same regions being those dysregulated in addiction. Moreover, in addicted adults, we propose that parenting cues trigger stress reactivity rather than reward salience, and this may heighten negative affect states, eliciting both addictive behaviors and the potential for child neglect and abuse.

Parental reflective functioning is associated with tolerance of infant distress but not general distress: Evidence for a specific relationship using a simulated baby paradigm

Parental reflective functioning represents the capacity of a parent to think about their own and their childs mental states and how these mental states may influence behavior. Here we examined whether this capacity as measured by the Parental Reflective Functioning Questionnaire relates to tolerance of infant distress by asking mothers (N = 21) to soothe a life-like baby simulator (BSIM) that was inconsolable, crying for a fixed time period unless the mother chose to stop the interaction. Increasing maternal interest and curiosity in their childs mental states, a key feature of parental reflective functioning, was associated with longer persistence times with the BSIM. Importantly, on a non-parent distress tolerance task, parental reflective functioning was not related to persistence times. These findings suggest that parental reflective functioning may be related to tolerance of infant distress, but not distress tolerance more generally, and thus may reflect specificity to persistence behaviors in parenting contexts.

Regional Brain Responses in Nulliparous Women to Emotional Infant Stimuli

Infant cries and facial expressions influence social interactions and elicit caretaking behaviors from adults. Recent neuroimaging studies suggest that neural responses to infant stimuli involve brain regions that process rewards. However, these studies have yet to investigate individual differences in tendencies to engage or withdraw from motivationally relevant stimuli. To investigate this, we used event-related fMRI to scan 17 nulliparous women. Participants were presented with novel infant cries of two distress levels (low and high) and unknown infant faces of varying affect (happy, sad, and neutral) in a randomized, counter-balanced order. Brain activation was subsequently correlated with scores on the Behavioral Inhibition System/Behavioral Activation System scale. Infant cries activated bilateral superior and middle temporal gyri (STG and MTG) and precentral and postcentral gyri. Activation was greater in bilateral temporal cortices for low- relative to high-distress cries. Happy relative to neutral faces activated the ventral striatum, caudate, ventromedial prefrontal, and orbitofrontal cortices. Sad versus neutral faces activated the precuneus, cuneus, and posterior cingulate cortex, and behavioral activation drive correlated with occipital cortical activations in this contrast. Behavioral inhibition correlated with activation in the right STG for high- and low-distress cries relative to pink noise. Behavioral drive correlated inversely with putamen, caudate, and thalamic activations for the comparison of high-distress cries to pink noise. Reward-responsiveness correlated with activation in the left precentral gyrus during the perception of low-distress cries relative to pink noise. Our findings indicate that infant cry stimuli elicit activations in areas implicated in auditory processing and social cognition. Happy infant faces may be encoded as rewarding, whereas sad faces activate regions associated with empathic processing. Differences in motivational tendencies may modulate neural responses to infant cues.

Attachment dismissal predicts frontal slow-wave ERPs during rejection by unfamiliar peers.

Attachment representations are thought to provide a cognitive-affective template, guiding the way individuals interact with unfamiliar social partners. To examine the neural correlates of this process, we sampled event-related potentials (ERPs) during exclusion by unfamiliar peers to differentiate insecure-dismissing from securely attached youth, as indexed by the child attachment interview. Thirteen secure and 10 dismissing 11- to 15-year-olds were ostensibly connected with two peers via the Internet to play a computerized ball-toss game. Actually, peers were computer generated, first distributing the ball evenly, but eventually excluding participants. Afterward children rated their distress. As in previous studies, distress was related to a negative left frontal slow wave (500-900 ms) during rejection, a waveform implicated in negative appraisals and less approach motivation. Though attachment classifications were comparable in frontal ERPs and distress, an attachment-related dismissal dimension predicted a negative left frontal slow wave during rejection, suggesting that high dismissal potentially involves elevated anticipation of rejection. As expected, dismissal and self-reported distress were uncorrelated. Yet, a new approach to quantifying the dissociation between self-reports and rejection-related ERPs revealed that dismissal predicted underreporting of distress relative to ERPs. Our findings imply that evaluations and regulatory strategies linked to attachment generalize to distressing social contexts in early adolescence.

Neurobiology of Adolescent Substance Use Disorders: Implications for Prevention and Treatment

Adolescence represents a unique period of development with neuronal maturation accompanied by increases in behavioral risk taking. Although risky behavior is a likely marker of normative adolescent development, there is an early emergence of substance use disorders in this population. Adolescence represents a distinct period of vulnerability to substance use initiation and transitions to substance abuse and dependence. Of recent interest is understanding the neurobiology of adolescent substance use disorders, with adult studies being limited in their applicability to this developmentally sensitive maturation period and providing restricted insight into potential treatment and intervention. First, the authors review the neurobiology of adolescent substance use disorders and, second, the authors consider the implications of these findings for prevention and treatment.

Investigating the impact of parental status and depression symptoms on the early perceptual coding of infant faces: An event-related potential study

Infant faces are highly salient social stimuli that appear to elicit intuitive parenting behaviors in healthy adult women. Behavioral and observational studies indicate that this effect may be modulated by experiences of reproduction, caregiving, and psychiatric symptomatology that affect normative attention and reward processing of infant cues. However, relatively little is known about the neural correlates of these effects. Using the event-related potential (ERP) technique, this study investigated the impact of parental status (mother, non-mother) and depression symptoms on early visual processing of infant faces in a community sample of adult women. Specifically, the P1 and N170 ERP components elicited in response to infant face stimuli were examined. While characteristics of the N170 were not modulated by parental status, a statistically significant positive correlation was observed between depression symptom severity and N170 amplitude. This relationship was not observed for the P1. These results suggest that depression symptoms may modulate early neurophysiological responsiveness to infant cues, even at sub-clinical levels.

Investigating the association between parental reflective functioning and distress tolerance in motherhood

Parental reflective functioning, referring to the capacity of a parent to consider their childs mental states as they relate to their behavior, may support sensitive and adaptive parenting. We investigated the relationship between parental reflective functioning and tolerance of distress in a sample of recent mothers (N=59). Participants completed self-report measures of parental reflective functioning and distress tolerance, as well as two behavioral distress tolerance tasks. We also examined blood pressure and heart rate during the laboratory session. Mothers reporting more difficulty in recognizing and understanding their childs mental states displayed decreased tolerance of distress on our behavioral and self-report measures. Further, we found evidence of a relationship between these measures and assessments of peripheral physiology. These findings are discussed in the context of reflective functioning and distress tolerance in parenthood, and their implications for parenting interventions.

Diminished social reward anticipation in the broad autism phenotype as revealed by event-related brain potentials

Diminished responsivity to reward incentives is a key contributor to the social-communication problems seen in autism spectrum disorders (ASDs). Social motivation theories suggest that individuals with ASD do not experience social interactions as rewarding, leading to negative consequences for the development of brain circuitry subserving social information. In this study, we examined neural responses to social and non-social reward anticipation in 35 typically developing young adults, examining modulation of reward sensitivity by level of autistic traits. Using an Event-related potential incentive-delay task incorporating novel, more ecologically valid forms of reward, higher expression of autistic traits was associated with an attenuated P3 response to the anticipation of social (simulated real-time video feedback from an observer), but not non-social (candy), rewards. Exploratory analyses revealed that this was unrelated to mentalizing ability. The P3 component reflects motivated attention to reward signals, suggesting attenuated motivation allocation specific to social incentives. The study extends prior findings of atypical reward anticipation in ASD, demonstrating that attenuated social reward responsiveness extends to autistic traits in the range of typical functioning. Results support the development of innovative paradigms for investigating social and non-social reward responsiveness. Insight into vulnerabilities in reward processing is critical for understanding social function in ASD.