Brain structural concomitants of resting state heart rate variability in the young and old: evidence from two independent samples.

Previous research has shown associations between brain structure and resting state high-frequency heart rate variability (HF HRV). Age affects both brain structure and HF HRV. Therefore, we sought to examine the relationship between brain structure and HF HRV as a function of age. Data from two independent studies were used for the present analysis. Study 1 included 19 older adults (10 males, age range 62-78 years) and 19 younger adults (12 males, age range 19-37). Study 2 included 23 older adults (12 males; age range 55-75) and 27 younger adults (17 males; age range 18-34). The root-mean-square of successive R-R-interval differences (RMSSD) from ECG recordings was used as time-domain measure of HF HRV. MRI scans were performed on a 3.0-T Siemens Magnetom Trio scanner. Cortical reconstruction and volumetric segmentation were performed with the Freesurfer image analysis suite, including 12 regions as regions of interests (ROI). Zero-order and partial correlations were used to assess the correlation of RMSSD with cortical thickness in selected ROIs. Lateral orbitofrontal cortex (OFC) cortical thickness was significantly associated with RMSSD. Further, both studies, in line with previous research, showed correlations between RMSSD and anterior cingulate cortex (ACC) cortical thickness. Meta-analysis on adjusted correlation coefficients from individual studies confirmed an association of RMSSD with the left rostral ACC and the left lateral OFC. Future longitudinal studies are necessary to trace individual trajectories in the association of HRV and brain structure across aging.

Heart rate variability is associated with amygdala functional connectivity with MPFC across younger and older adults.

The ability to regulate emotion is crucial to promote well-being. Evidence suggests that the medial prefrontal cortex (mPFC) and adjacent anterior cingulate (ACC) modulate amygdala activity during emotion regulation. Yet less is known about whether the amygdala-mPFC circuit is linked with regulation of the autonomic nervous system and whether the relationship differs across the adult lifespan. The current study tested the hypothesis that heart rate variability (HRV) reflects the strength of mPFC-amygdala interaction across younger and older adults. We recorded participants' heart rates at baseline and examined whether baseline HRV was associated with amygdala-mPFC functional connectivity during rest. We found that higher HRV was associated with stronger functional connectivity between the amygdala and the mPFC during rest across younger and older adults. In addition to this age-invariant pattern, there was an age-related change, such that greater HRV was linked with stronger functional connectivity between amygdala and ventrolateral PFC (vlPFC) in younger than in older adults. These results are in line with past evidence that vlPFC is involved in emotion regulation especially in younger adults. Taken together, our results support the neurovisceral integration model and suggest that higher heart rate variability is associated with neural mechanisms that support successful emotional regulation across the adult lifespan.

Age-related similarities and differences in brain activity underlying reversal learning.

The ability to update associative memory is an important aspect of episodic memory and a critical skill for social adaptation. Previous research with younger adults suggests that emotional arousal alters brain mechanisms underlying memory updating; however, it is unclear whether this applies to older adults. Given that the ability to update associative information declines with age, it is important to understand how emotion modulates the brain processes underlying memory updating in older adults. The current study investigated this question using reversal learning tasks, where younger and older participants (age ranges 19-35 and 61-78, respectively) learn a stimulus-outcome association and then update their response when contingencies change. We found that younger and older adults showed similar patterns of activation in the frontopolar OFC and the amygdala during emotional reversal learning. In contrast, when reversal learning did not involve emotion, older adults showed greater parietal cortex activity than did younger adults. Thus, younger and older adults show more similarities in brain activity during memory updating involving emotional stimuli than during memory updating not involving emotional stimuli.

Age differences in thalamic low-frequency fluctuations.

The thalamus plays a role in many different types of cognitive processes and is critical for communication between disparate cortical regions. Given its critical role in coordinating cognitive processes, it is important to understand how its function might be affected by aging. In the present study, we examined whether there are age differences in low-frequency fluctuations during rest in the thalamus. Across independent data sets, we found that the amplitude of low-frequency (0.01-0.10 Hz) oscillations was greater in the thalamus among older than younger adults. Breaking this low-frequency range down further revealed that this increase in amplitude with age in the thalamus was most pronounced at the low end of the frequency range (0.010-0.027 Hz), whereas in the higher low-frequency range (0.198-0.250 Hz) younger adults showed greater amplitude than older adults. These shifts in thalamic low-frequency oscillatory activity likely influence the complex dynamics of coordinated brain activity and influence cognitive performance.

Amygdala functional connectivity with medial prefrontal cortex at rest predicts the positivity effect in older adults' memory.

As people get older, they tend to remember more positive than negative information. This age-by-valence interaction has been called "positivity effect." The current study addressed the hypotheses that baseline functional connectivity at rest is predictive of older adults' brain activity when learning emotional information and their positivity effect in memory. Using fMRI, we examined the relationship among resting-state functional connectivity, subsequent brain activity when learning emotional faces, and individual differences in the positivity effect (the relative tendency to remember faces expressing positive vs. negative emotions). Consistent with our hypothesis, older adults with a stronger positivity effect had increased functional coupling between amygdala and medial PFC (MPFC) during rest. In contrast, younger adults did not show the association between resting connectivity and memory positivity. A similar age-by-memory positivity interaction was also found when learning emotional faces. That is, memory positivity in older adults was associated with (a) enhanced MPFC activity when learning emotional faces and (b) increased negative functional coupling between amygdala and MPFC when learning negative faces. In contrast, memory positivity in younger adults was related to neither enhanced MPFC activity to emotional faces, nor MPFC-amygdala connectivity to negative faces. Furthermore, stronger MPFC-amygdala connectivity during rest was predictive of subsequent greater MPFC activity when learning emotional faces. Thus, emotion-memory interaction in older adults depends not only on the task-related brain activity but also on the baseline functional connectivity.

Differential brain activity during emotional versus nonemotional reversal learning.

The ability to change an established stimulus-behavior association based on feedback is critical for adaptive social behaviors. This ability has been examined in reversal learning tasks, where participants first learn a stimulus-response association (e.g., select a particular object to get a reward) and then need to alter their response when reinforcement contingencies change. Although substantial evidence demonstrates that the OFC is a critical region for reversal learning, previous studies have not distinguished reversal learning for emotional associations from neutral associations. The current study examined whether OFC plays similar roles in emotional versus neutral reversal learning. The OFC showed greater activity during reversals of stimulus-outcome associations for negative outcomes than for neutral outcomes. Similar OFC activity was also observed during reversals involving positive outcomes. Furthermore, OFC activity is more inversely correlated with amygdala activity during negative reversals than during neutral reversals. Overall, our results indicate that the OFC is more activated by emotional than neutral reversal learning and that OFC's interactions with the amygdala are greater for negative than neutral reversal learning.

Gender differences in reward-related decision processing under stress.

Recent research indicates gender differences in the impact of stress on decision behavior, but little is known about the brain mechanisms involved in these gender-specific stress effects. The current study used functional magnetic resonance imaging (fMRI) to determine whether induced stress resulted in gender-specific patterns of brain activation during a decision task involving monetary reward. Specifically, we manipulated physiological stress levels using a cold pressor task, prior to a risky decision making task. Healthy men (n = 24, 12 stressed) and women (n = 23, 11 stressed) completed the decision task after either cold pressor stress or a control task during the period of cortisol response to the cold pressor. Gender differences in behavior were present in stressed participants but not controls, such that stress led to greater reward collection and faster decision speed in males but less reward collection and slower decision speed in females. A gender-by-stress interaction was observed for the dorsal striatum and anterior insula. With cold stress, activation in these regions was increased in males but decreased in females. The findings of this study indicate that the impact of stress on reward-related decision processing differs depending on gender.

Negative emotional outcomes impair older adults' reversal learning.

In a typical reversal-learning experiment, one learns stimulus-outcome contingencies that then switch without warning. For instance, participants might have to repeatedly choose between two faces, one of which yields points whereas the other does not, with a reversal at some point in which face yields points. The current study examined age differences in the effects of outcome type on reversal learning. In the first experiment, the participants' task was either to select the person who would be in a better mood or to select the person who would yield more points. Reversals in which face was the correct option occurred several times. Older adults did worse in blocks in which the correct response was to select the person who would not be angry than in blocks in which the correct response was to select the person who would smile. Younger adults did not show a difference by emotional valence. In the second study, the negative condition was switched to have the same format as the positive condition (to select who will be angry). Again, older adults did worse with negative than positive outcomes, whereas younger adults did not show a difference by emotional valence. A third experiment replicated the lack of valence effects in younger adults with a harder probabilistic reversal-learning task. In the first two experiments, older adults performed about as well as younger adults in the positive conditions but performed worse in the negative conditions. These findings suggest that negative emotional outcomes selectively impair older adults' reversal learning.

Sex differences in how stress affects brain activity during face viewing.

Under stress, men tend to withdraw socially whereas women seek social support. This functional magnetic resonance imaging study indicates that stress also affects brain activity while viewing emotional faces differently for men and women. Fusiform face area response to faces was diminished by acute stress in men but increased by stress in women. Furthermore, among stressed men viewing angry faces, brain regions involved in interpreting and understanding others' emotions (the insula, temporal pole, and inferior frontal gyrus) showed reduced coordination with the fusiform face area and the amygdala, whereas the functional connectivity among these regions increased with stress for women. These findings suggest that stress influences emotional perception differently for men and women.