Frontostriatal circuitry as a target for fMRI-based neurofeedback interventions: A systematic review

Abstract

Dysregulated frontostriatal circuitries are viewed as a common target for the treatment of aberrant behaviors in various psychiatric and neurological disorders. Accordingly, experimental neurofeedback paradigms have been applied to modify the frontostriatal circuitry. The human frontostriatal circuitry is topographically and functionally organized into the "limbic," the "associative," and the "motor" subsystems underlying a variety of affective, cognitive, and motor functions. We conducted a systematic review of the literature regarding functional magnetic resonance imaging-based neurofeedback studies that targeted brain activations within the frontostriatal circuitry. Seventy-nine published studies were included in our survey. We assessed the efficacy of these studies in terms of imaging findings of neurofeedback intervention as well as behavioral and clinical outcomes. Furthermore, we evaluated whether the neurofeedback targets of the studies could be assigned to the identifiable frontostriatal subsystems. The majority of studies that targeted frontostriatal circuitry functions focused on the anterior cingulate cortex, the dorsolateral prefrontal cortex, and the supplementary motor area. Only a few studies (n = 14) targeted the connectivity of the frontostriatal regions. However, post-hoc analyses of connectivity changes were reported in more cases (n = 32). Neurofeedback has been frequently used to modify brain activations within the frontostriatal circuitry. Given the regulatory mechanisms within the closed loop of the frontostriatal circuitry, the connectivity-based neurofeedback paradigms should be primarily considered for modifications of this system. The anatomical and functional organization of the frontostriatal system needs to be considered in decisions pertaining to the neurofeedback targets.

Keywords: connectivity neurofeedback; frontostriatal circuitry; neurofeedback; neuromodulation; real-time fMRI.

Figure 1

Three-part organization of the frontostriatal circuitry with distinct “limbic” (A), “associative” (B), and “motor” (C) subsystems linking the frontal cortical regions and the striatum. (A) The “limbic” subsystem is divided into two parts. The first part originates in the lateral orbitofrontal cortex (OFC) and projects to the ventromedial sector of the caudate nucleus. This region innervates the dorsomedial globus pallidus interna (GPi) and rostromedial substantia nigra (SNr, not shown). The latter projects to the ventral anterior thalamic nucleus, magnocellular part and the mediodorsal thalamic nucleus, magnocellular part before it forms a closed loop with the lateral OFC. Both the anterior cingulate cortex (ACC) and medial OFC project to the ventral striatum (ventromedial caudate, ventral putamen, nucleus accumbens and olfactory tubercle) which in turn project to the rostrolateral GPi and the rostrodorsal SNr. Via the mediodorsal thalamic nucleus, magnocellular part, the SNr sends fibers back to the ACC and medial OFC. (B) Within the “associative” subsystem, the dorsolateral prefrontal cortex (DLPFC) projections terminate in the dorsolateral head of the caudate nucleus. The caudate nucleus projects to the dorsomedial part of the GPi and globus pallidus externa (GPe) and from there to the rostral portions of the SNr. The GPi closes the loop via the parvocellular portion of the ventral anterior thalamic nucleus to the DLPFC. (C) Motor-relevant cortical areas (motor, premotor, supplementary motor, and somatosensory cortices) innervate the caudal putamen, which sends input to the ventrolateral GPi and GPe and to the caudolateral portions of the SNr. The GPi sends input to the ventrolateral nucleus of the thalamus, which in turns forms a closed loop with the motor cortex. In all three subsystems, the subthalamic nucleus (STN) modulates input to the thalamus via the GPi and/or GPe. a, anterior; p, posterior; m, medial; l, lateral. This figure adapted from Obeso et al. (2008).

Figure 2

PRISMA flow diagram of the literature search (adapted from Moher et al., 2009).

Figure 3

Distribution of study populations in the selected publications. ADHD, attention deficit hyperactivity disorder; PTSD, post-traumatic stress disorder; SUD, substance-use disorders.

Figure 4

Targets within the frontostriatal circuitry (FSC) for fMRI-based NF in clinical populations. This graph depicts the targeted regions within the FSC for the three subsystems. The circle, square, and triangle refer to the regions in limbic, associative, and motor subsystems, respectively. The dashed line represents connectivity feedback. Regions outside the FSC with connectivity feedback to FSC regions are marked in gray. ACC, anterior cingulate cortex; ADHD, attention deficits hyperactivity disorder; DLPFC, dorsolateral prefrontal cortex; HD, Huntington's disease; IFG, inferior frontal gyrus; M1, primary motor cortex; MPFC, medial prefrontal cortex; OFC, orbitofrontal cortex; PCC, posterior cingulate cortex; PD, Parkinson's disease; PMA, premotor area; PTSD, post-traumatic stress disorder; SATL, superior anterior temporal lobe; sgACC, subgenual cingulate; SMA, supplementary motor area; SUD, substance-use disorders; VS, ventral striatum; VLPFC, ventrolateral prefrontal cortex.