Anterior Cingulate Cortex Modulation of the Ventral Tegmental Area in an Effort Task

Elston, Thomas W; Bilkey, David K.

doi:10.1016/j.celrep.2017.05.062

Cited by 49 publications

(57 citation statements)

References 61 publications

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“…This model is also characterized by VTA hyperactivity, and normalizing VTA hyperconnectivity reduces the depressive, anhedonic phenotype (38). Another recent preclinical study has demonstrated that VTA connectivity with ACC mediates motivation for rewards (39) and heightened subgenual ACC connectivity has been previously demonstrated in patients with MDD (40). The current translational study confirms the observation of VTA hyperconnectivity in humans with depression who are free of medication.…”

Section: Discussionsupporting

confidence: 83%

Ultra-high field MRI reveals mood-related circuit disturbances in depression: A comparison between 3-Tesla and 7-Tesla

Morris

Kundu

Costi

et al. 2018

Preprint

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Ultra-high field 7-Tesla (7T) MRI has the potential to advance our understanding of neuropsychiatric disorders, including major depressive disorder (MDD). To date, few studies have quantified the advantage of resting state functional MRI (fMRI) at 7T compared to 3-Tesla (3T). We conducted a series of experiments that systematically quantified the improvement in temporal signal-to-noise ratio (tSNR) of a multi-echo multi-band fMRI protocol with ultra-high field 7T, compared to 3T MRI in healthy controls (HC). We also directly tested the enhancement in ultra-high field 7T fMRI signal power by examining the ventral tegmental area (VTA), a small midbrain structure that is critical to the expected neuropathology of MDD but difficult to discern with standard 3T MRI. We demonstrate 200-300% improvement in tSNR and resting state functional connectivity metrics provided by ultra-high field 7T fMRI compared to the same imaging protocol with 3T, indicating enhanced power for detection of functional architecture. A multi-echo based acquisition protocol and signal denoising pipeline afforded greater gain in signal power at ultra-high field compared to classic acquisition and denoising pipelines. Furthermore, ultra-high field fMRI revealed mood-related neuro-circuit disturbances in patients with MDD compared to HC, which weren't detectable with 3T fMRI. Ultra-high field 7T fMRI may provide an effective tool for studying functional neural architecture relevant to MDD and other neuropsychiatric disorders.

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Section: Discussionsupporting

confidence: 83%

Ultra-high field MRI reveals mood-related circuit disturbances in depression: A comparison between 3-Tesla and 7-Tesla

Morris

Kundu

Costi

et al. 2018

Preprint

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“…The ACC and VTA power spectrum density (PSD) functions from 1 to 30 Hz obtained from this dataset ( Figure 3) were consistent with prior reports showing that the VTA and ACC exhibited local peaks centered at $4 Hz (Elston and Bilkey, 2017;Fujisawa and Buzsá ki, 2011;Parker et al, 2014). For comparison, we also computed the PSDs and coherence of the nine rats roaming in a familiar open field.…”

Section: Decision Patterns Running Speeds and Latenciessupporting

confidence: 85%

“…We also observed an 8-to 12-Hz oscillation in the VTA, which was sustained throughout the trials (see Figure 4). However, because activity within and between the ACC and VTA has been previously reported to occur at $4 Hz (Elston and Bilkey, 2017;Fujisawa and Buzsá ki, 2011;Gao et al, 2007;Parker et al, 2014;Parker et al, 2015), the 8-to 12-Hz frequency band did not significantly differ between the open field and task conditions. To retain focus in the current paper, we focused our subsequent analyses on 2to 5-Hz activity (referred to as 4 Hz throughout the rest of this paper).…”

Section: Decision Patterns Running Speeds and Latenciesmentioning

confidence: 69%

“…Anatomical, electrophysiological, and computational evidence suggests that the ACC could influence behavior via the monosynaptic glutamatergic afferents projecting to the ventral tegmental area (VTA), a midbrain dopaminergic structure implicated in motivation (Ballard et al, 2011;Carr and Sesack, 2000;Elston and Bilkey, 2017;Gao et al, 2007;Gariano and Groves, 1988;Holroyd and McClure, 2015;Holroyd and Yeung, 2012;Olds, 1958). For example, direct electrical stimulation of the ACC evokes burst firing in VTA dopamine neurons (Gariano and Groves, 1988), and transient increases in ACC-to-VTA signaling, modulated at $4 Hz, appear related to increases in motivation (Elston and Bilkey, 2017). Although these data indicate that ACC-to-VTA 4-Hz signaling is a plausible mechanism by which ACC neural activity could influence VTA-generated motivational signals, we know little about how the ACC and VTA might interact during decision making.…”

Section: Introductionmentioning

confidence: 99%

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Communication between the Anterior Cingulate Cortex and Ventral Tegmental Area during a Cost-Benefit Reversal Task

2019

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Graphical Abstract Highlights d Anticipatory decision making is associated with increased ACC/VTA signaling d Sustaining behavior toward a new default is associated with ACC/VTA signaling d Error-related feedback integration is associated with increased VTA/ACC signaling d Error-related VTA/ACC signaling is predictive of subsequent choice adaptation Correspondence telston@nurhopsi.org In Brief Elston et al. find that the initiation and persistence of non-default behavior are associated with increases in top-down, ACC-to-VTA signaling. Additionally, the authors show that error-related feedback integration and subsequent behavioral adaptation accompany increases in bottom-up, VTA-to-ACC signaling. These results indicate that bidirectional ACC-VTA signaling is important for behavioral flexibility. SUMMARYThe anterior cingulate cortex (ACC) is implicated in value-based decision making, anticipation, and adaptation; however, how ACC activity modulates these behaviors is unclear. One possibility is via the ACC's connections with the ventral tegmental area (VTA), a dopaminergic region implicated in motivation and feedback processing. We tested this by monitoring ACC and VTA local field potentials in rats performing a cost-benefit reversal task that elicited both value-based and anticipatory choices. Partial directed coherence analyses revealed that elevated 4-Hz ACC-to-VTA signaling accompanied decisions that appeared to be anticipatory. ACCto-VTA signaling also occurred post-reversal, consistent with it being involved in the initiation of non-default behavior. An analysis of 4-Hz signals in the other direction (VTA-to-ACC) revealed that it was elevated when the rats committed errors and that this signal was followed by behavioral adaptation. Together, these findings suggest that bidirectional communication between the ACC and VTA supports behavioral flexibility.

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“…In voles, the ACC has been implicated in regulating empathy-based consoling behavior towards the partner (Burkett et al, 2016). The VTA is a region known to modulate motivational, reward, and emotionally salient stimuli (Elston & Bilkey, 2017; Gunaydin et al, 2014). There is evidence that the VTA modulates DA release in prefrontal regions to regulate behaviorally relevant stimuli (Takahata & Moghaddam, 2002), including sexually relevant stimuli (Cortes et al, 2019).…”

Section: Discussionmentioning

confidence: 99%

Brain functional connectivity modulates social bonding in monogamous voles

Camacho

et al. 2019

Preprint

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Microtus ochrogaster, the prairie vole, has become a valuable rodent model to study complex social behaviors, including enduring social bonding. Previous studies have related pair bonding in the prairie vole with plastic changes in several brain regions. However, the network interaction between these regions and their relevance to such socio-sexual behaviors has yet to be described. In this study, we used resting state functional magnetic resonance imaging (rsfMRI) to explore the longitudinal changes in the functional interactions of a set of brain regions previously associated with pair bonding in prairie voles. Specifically, 32 prairie voles were scanned at baseline, after 24 hours and two weeks of cohabitation and mating with a sexual partner (16 male-female pairs). Between 48 and 72 hours of cohabitation voles showed significant preference for the partner over a stranger, confirming pair bond formation; however, individual variability was observed. Network based statistics showed no sex differences in functional connectivity, but revealed a common network with significant longitudinal changes between sessions, including the anterior cingulate cortex (ACC), anterior olfactory nucleus (AON), dentate gyrus (DG), dorsal hippocampus (dHIP), lateral septum (LS), medial prefrontal cortex (mPFC), retrosplenial cortex (RSC), ventral hippocampus (vHIP), and ventral tegmental area (VTA). Furthermore, baseline functional connectivity in three sub-networks including the ACC, nucleus accumbens (NAcc), basolateral amygdala, and DG (ACC-NAcc-BLA-DG), the medial amygdala (MeA)-ventral pallidum (VP), and RSC-VTA, predicted the onset of affiliative behavior (huddling latency) in the first hours of cohabitation, even before sexual experience. Finally, a relationship was found between the strength of the pair bond (partner preference index) with long-term changes in the functional connectivity between the ventral pallidum and medial amygdala (MeA-VP). Overall, our findings revealed the association between network-level changes and the process of social bonding, and provide a novel approach to further investigate the neurophysiology of complex social behaviors displayed in the prairie vole.

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Anterior Cingulate Cortex Modulation of the Ventral Tegmental Area in an Effort Task

Cited by 49 publications

References 61 publications

Ultra-high field MRI reveals mood-related circuit disturbances in depression: A comparison between 3-Tesla and 7-Tesla

Ultra-high field MRI reveals mood-related circuit disturbances in depression: A comparison between 3-Tesla and 7-Tesla

Communication between the Anterior Cingulate Cortex and Ventral Tegmental Area during a Cost-Benefit Reversal Task

Brain functional connectivity modulates social bonding in monogamous voles

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