Resting-state functional connectivity (rsFC) refers to the temporal correlation of spontaneous neural activity between distinct brain regions or networks when an individual is not engaged in any specific task [1]. RsFC provides valuable insights into intrinsic brain organization and is widely used to examine how neural networks interact in both healthy and clinical populations [2,3]. Studies utilizing rsFC have identified patterns of connectivity that underlie cognitive and emotional processes, highlighting its potential in understanding mental health outcomes [4]. Disruptions in rsFC have been linked to various neuropsychiatric disorders, including depression, anxiety, and substance use, making it a critical area of investigation in developmental neuroscience [5].

Corticostriatal connectivity, which encompasses functional interactions between the cortex and the striatum, is particularly important in regulating cognitive control, emotion, and reward-related behaviors [6–9]. This connectivity plays a vital role in goal-directed behavior, habit formation, and emotional regulation [10–12]. The corticostriatal pathway has been implicated in neurodevelopmental disorders, addiction, and psychiatric conditions, with variations in connectivity patterns observed across different socioeconomic and environmental contexts [13–15]. Understanding the factors that influence corticostriatal connectivity is crucial for identifying neurobiological mechanisms that contribute to health disparities and behavioral outcomes.

The caudate nucleus, a major component of the striatum, is involved in various cognitive functions, including decision-making, learning, and reward processing [16–19]. It plays a pivotal role in modulating goal-directed behavior and is integral to the corticostriatal circuitry [16,20–24]. Structural and functional abnormalities in the caudate have been associated with impulsivity, cognitive deficits, and increased vulnerability to substance use disorders. The caudate’s connectivity with cortical regions, particularly those involved in executive function and emotional regulation, provides critical insights into individual differences in cognitive and affective processing.

In 1989, Mendez et al. [25] was among the first to highlight the role of the caudate nucleus in behavior. The study examined 12 patients with caudate lesions—11 unilateral and one bilateral—and documented significant behavioral and cognitive changes. Patients exhibited acute behavioral alterations, including apathy, disinhibition, or major affective disturbances. The nature of personality changes was found to be associated with the size and location of the lesion within the caudate, rather than its laterality. A subset of seven patients was further assessed using neuropsychological tests and compared with matched controls. Those with caudate lesions demonstrated deficits in tasks requiring planning and sequencing, exhibited short attention spans, and showed reduced free recall for episodic and semantic information, despite intact recognition memory. Similar cognitive and behavioral impairments have been observed in individuals with early Huntington’s disease, frontal lobe damage, and caudate lesions in animal models, suggesting disruptions in specific frontal-caudate circuits. These findings provided early evidence of the caudate’s role in prefrontal-mediated behaviors and the conceptual integration of memory. Subsequent studies have since reinforced these findings, further establishing the role of caudate dysfunction in behavioral, cognitive, and memory disturbances [25–28].

A meta-analytic connectivity modeling (MACM) approach [29] was utilized to examine the functional connectivity of the human caudate. The study aimed to: (1) construct a model of functional connectivity, (2) assess whether meta-analytic techniques are sensitive enough to identify behavioral domain specificity within region-specific connectivity networks, and (3) compare meta-analytically derived segmentation with structural connectivity parcellation obtained through diffusion tensor imaging (DTI). The findings indicated that behavioral filtering distinguished cognition- and emotion-related structures and networks, primarily concentrated in the head of the caudate nucleus, while regions associated with perception and action were localized to the body of the caudate. These results align with earlier histological studies in nonhuman primates and postmortem research in humans. Additionally, DTI findings supported the utility of MACM in detecting both direct and indirect connectivity patterns. Overall, the study provided further validation for MACM while demonstrating its potential to extract behavioral domain-specific functional connectivity [29].

The human dorsal striatum serves as the primary input region to the basal ganglia [21,30–33]. Comprising the caudate and putamen, it receives projections from nearly all cortical areas, except for the primary visual, auditory, and olfactory cortices [34]. Structural, functional, and connectivity alterations in the caudate nucleus have been observed in various neuropsychiatric conditions, including depression [35], attention deficit disorders [36], and substance addiction [37,38].

In their review paper, Jessica Grahn and colleagues explored the distinct functional roles of the caudate nucleus and the putamen. Their analysis integrated findings from multiple domains, including anatomical studies of corticostriatal pathways, neuroimaging research on healthy individuals, patient studies examining cognitive deficits, and animal research on behavioral regulation. They concluded that the caudate nucleus plays a key role in facilitating behavior by activating appropriate action schemas and selecting sub-goals based on action-outcome evaluations—both essential for goal-directed behavior. In contrast, putamen was primarily associated with cognitive processes related to stimulus-response learning and habit formation. Their findings support a modular framework of striatal function, aligning with hierarchical models of cortico-striatal processing, in which the ventral striatum is linked to motivation, the caudate to cognitive planning, and the putamen to sensorimotor execution, collectively enabling adaptive goal-directed behavior [21].

The cingulo-opercular network [39–41]is a core cognitive control network that includes regions such as the anterior cingulate cortex (ACC), insula, and frontal operculum [42–44]. This network is responsible for maintaining task performance, error monitoring, and adaptive control in response to changing environmental demands [45–47]. It has been shown to be involved in sustained attention, emotional regulation, and self-monitoring processes. Alterations in cingulo-opercular network connectivity have been linked to mood disorders, impulsivity, and substance use behaviors, highlighting its relevance in understanding the interplay between brain function and psychosocial factors.

RsFC between the left caudate and the cingulo-opercular network, here referred to as corticostriatal connectivity, may play a role in cognitive and affective processes. This connectivity is linked to various psychosocial and behavioral factors, including socioeconomic status (SES), trauma exposure, cognitive function, reward salience, impulsivity, and future substance use. Investigating these associations can provide insights into how environmental and individual factors interact with neurobiological mechanisms to influence mental health and behavioral outcomes over time.

This study investigates the associations between left caudate-cingulo-opercular connectivity and multiple domains, including low SES, high trauma exposure (financial and life events), cognitive function, reward salience, impulsivity, depression, and future substance use (tobacco and marijuana use). The following hypotheses were examined: (1) lower SES and higher trauma exposure will be associated with altered corticostriatal connectivity, (2) variations in corticostriatal connectivity will predict differences in cognitive function, impulsivity, and reward salience, and (3) disrupted corticostriatal connectivity at baseline will be linked to increased risk of future tobacco and marijuana use. These findings aim to contribute to a better understanding of the neurobiological underpinnings of health disparities and substance use vulnerability in youth.