Experience selectively alters functional connectivity within a neural network to predict learned behavior in juvenile songbirds.

One of the central questions of neuroethology is how specialized brain areas communicate to form dynamic networks that support complex cognitive and behavioral processes. Developmental song learning in the male zebra finch songbird (Taeniopygia guttata) provides a unique window into the complex interplay among sensory, sensorimotor, and motor network nodes. The foundation of a young male's song structure is the sensory memory he forms during interactions with an adult "tutor." However, even in the absence of tutoring, juveniles produce a song-like behavior. Thus, by controlling a juvenile male's tutor exposure, we can examine how tutor experience affects distributed neural networks and how network properties predict behavior. Here, we used longitudinal, resting-state fMRI (rs-fMRI) functional connectivity (FC) and song analyses to examine known nodes of the song network, and to allow discovery of additional areas functionally related to song learning. We present three major novel findings. First, tutor deprivation significantly reduced the global FC strength of the caudomedial nidopallium (NCM) subregion of the auditory forebrain required for sensory song learning. Second, tutor deprivation resulted in reduced FC between NCM and cerebellar lobule VI, a region analogous to areas that regulate limbic, social, and language functions in humans. Third, NCM FC strength predicted song stereotypy and mediated the relationship between tutoring and stereotypy, thus completing the link between experience, neural network properties, and complex learned behavior.

Interhemispheric functional connectivity in the zebra finch brain, absent the corpus callosum in normal ontogeny.

Bilaterally symmetric intrinsic brain activity (homotopic functional connectivity; FC) is a fundamental feature of the mammalian brain's functional architecture. In mammals, homotopic FC is primarily mediated by the corpus callosum (CC), a large interhemispheric white matter tract thought to balance the bilateral coordination and hemispheric specialization critical for many complex brain functions, including human language. The CC first emerged with the Eutherian (placental) mammals ∼160 MYA and is not found among other vertebrates. Despite this, other vertebrates also exhibit complex brain functions requiring hemispheric specialization and coordination. For example, the zebra finch (Taeniopygia guttata) songbird learns to sing from tutors much as humans acquire speech and must balance hemispheric specialization and coordination to successfully learn and produce song. We therefore tested whether the zebra finch also exhibits homotopic FC, despite lacking the CC. Resting-state fMRI analyses demonstrated widespread homotopic FC throughout the zebra finch brain across development, including within a network required for learned song that lacks direct interhemispheric structural connectivity. The presence of homotopic FC in a non-Eutherian suggests that ancestral pathways, potentially including indirect connectivity via the anterior commissure, are sufficient for maintaining a homotopic functional architecture, an insight with broad implications for understanding interhemispheric coordination across phylogeny.

Functional connectivity of reflective and brooding rumination in depressed and healthy women.

Ruminative thinking is related to an increased risk for major depressive disorder (MDD) and perpetuates negative mood states. Rumination, uncontrollable negative thoughts about the self, may comprise both reflective and brooding components. However, only brooding rumination is consistently associated with increased negativity bias and negative coping styles, while reflective rumination has a less clear relationship with negative outcomes in healthy and depressed participants. The current study examined seed-to-voxel (S2.V) resting-state functional connectivity (FC) in a sample of healthy (HC) and depressed (MDD) adult women (HC: n=50, MDD: n=33). The S2V FC of six key brain regions, including the left and right amygdala, anterior and posterior cingulate cortex (ACC, PCC), and medial and dorsolateral prefrontal cortices (mPFC, dlPFC), was correlated with self-reported reflective and brooding rumination. Results indicate that HC and MDD participants had increased brooding rumination associated with decreased FC between the left amygdala and the right temporal pole. Moreover, reflective rumination was associated with distinct FC of the mPFC, PCC, and ACC with parietal, occipital, and cingulate regions. Depressed participants, compared with HC, exhibited decreased FC between the PCC and a region in the right middle frontal gyrus. The results of the current study add to the understanding of the neural underpinnings of different forms of self-related cognition-brooding and reflective rumination-in healthy and depressed women.

Perceived social isolation is associated with altered functional connectivity in neural networks associated with tonic alertness and executive control.

Perceived social isolation (PSI), colloquially known as loneliness, is associated with selectively altered attentional, cognitive, and affective processes in humans, but the neural mechanisms underlying these adjustments remain largely unexplored. Behavioral, eye tracking, and neuroimaging research has identified associations between PSI and implicit hypervigilance for social threats. Additionally, selective executive dysfunction has been evidenced by reduced prepotent response inhibition in social Stroop and dichotic listening tasks. Given that PSI is associated with pre-attentional processes, PSI may also be related to altered resting-state functional connectivity (FC) in the brain. Therefore, we conducted the first resting-state fMRI FC study of PSI in healthy young adults. Five-minute resting-state scans were obtained from 55 participants (31 females). Analyses revealed robust associations between PSI and increased brain-wide FC in areas encompassing the right central operculum and right supramarginal gyrus, and these associations were not explained by depressive symptomatology, objective isolation, or demographics. Further analyses revealed that PSI was associated with increased FC between several nodes of the cingulo-opercular network, a network known to underlie the maintenance of tonic alertness. These regions encompassed the bilateral insula/frontoparietal opercula and ACC/pre-SMA. In contrast, FC between the cingulo-opercular network and right middle/superior frontal gyrus was reduced, a finding associated with diminished executive function in prior literature. We suggest that, in PSI, increased within-network cingulo-opercular FC may be associated with hypervigilance to social threat, whereas reduced right middle/superior frontal gyrus FC to the cingulo-opercular network may be associated with diminished impulse control.

Improvements in task performance after practice are associated with scale-free dynamics of brain activity.

Although practicing a task generally benefits later performance on that same task, there are individual differences in practice effects. One avenue to model such differences comes from research showing that brain networks extract functional advantages from operating in the vicinity of criticality, a state in which brain network activity is more scale-free. We hypothesized that higher scale-free signal from fMRI data, measured with the Hurst exponent (H), indicates closer proximity to critical states. We tested whether individuals with higher H during repeated task performance would show greater practice effects. In Study 1, participants performed a dual-n-back task (DNB) twice during MRI (n = 56). In Study 2, we used two runs of n-back task (NBK) data from the Human Connectome Project sample (n = 599). In Study 3, participants performed a word completion task (CAST) across six runs (n = 44). In all three studies, multivariate analysis was used to test whether higher H was related to greater practice-related performance improvement. Supporting our hypothesis, we found patterns of higher H that reliably correlated with greater performance improvement across participants in all three studies. However, the predictive brain regions were distinct, suggesting that the specific spatial H↑ patterns are not task-general.

Loneliness predicts a preference for larger interpersonal distance within intimate space.

Loneliness is thought to serve as an adaptive signal indicating the need to repair or replace salutary social connections. Accordingly, loneliness may influence preferences for interpersonal distance. If loneliness simply motivates a desire to socially reconnect, then loneliness may be associated with a preference for smaller interpersonal distances. According to the evolutionary model of loneliness, however, loneliness also signals an inadequacy of mutual aid and protection, augmenting self-preservation motives. If loneliness both increases the motivation to reconnect and increases the motivation for self-protection, then the resulting approach-avoidance conflict should produce a preference for larger interpersonal distance, at least within intimate (i.e., proximal) space. Here, we report two survey-based studies of participants' preferences for interpersonal distance to distinguish between these competing hypotheses. In Study 1 (N = 175), loneliness predicted preferences for larger interpersonal distance within intimate space net gender, objective social isolation, anxiety, depressive symptomatology, and marital status. In Study 2 (N = 405), we replicated these results, and mediation analyses indicated that measures of social closeness could not adequately explain our findings. These studies provide compelling evidence that loneliness predicts preferences for larger interpersonal distance within intimate space, consistent with predictions from the evolutionary model of loneliness.