The Will to Persevere Induced by Electrical Stimulation of the Human Cingulate Gyrus

Parvizi, Josef; Rangarajan, Vinitha; Shirer, William R.; Desai, Nikita; Greicius, Michael D.

doi:10.1016/j.neuron.2013.10.057

Cited by 208 publications

(164 citation statements)

References 31 publications

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“…External support for an invigorating function comes from related work on dopamine showing that it broadcasts a motivational signal (16,71) that in turn influences vigor (72)(73)(74). Interestingly, direct phenomenological support for such a motivational signal comes from observations in human subjects undergoing electrical stimulation of cingulate cortex, who report a motivational urge and a determination to overcome effort (75).…”

Section: Discussionmentioning

confidence: 99%

Separate mesocortical and mesolimbic pathways encode effort and reward learning signals

Hauser

Eldar

Dolan

2017

Proc. Natl. Acad. Sci. U.S.A.

120

127

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Optimal decision making mandates organisms learn the relevant features of choice options. Likewise, knowing how much effort we should expend can assume paramount importance. A mesolimbic network supports reward learning, but it is unclear whether other choice features, such as effort learning, rely on this same network. Using computational fMRI, we show parallel encoding of effort and reward prediction errors (PEs) within distinct brain regions, with effort PEs expressed in dorsomedial prefrontal cortex and reward PEs in ventral striatum. We show a common mesencephalic origin for these signals evident in overlapping, but spatially dissociable, dopaminergic midbrain regions expressing both types of PE. During action anticipation, reward and effort expectations were integrated in ventral striatum, consistent with a computation of an overall net benefit of a stimulus. Thus, we show that motivationally relevant stimulus features are learned in parallel dopaminergic pathways, with formation of an integrated utility signal at choice. effort prediction errors | reward prediction errors | apathy | substantia nigra/ventral tegmental area | dorsomedial prefrontal cortex O rganisms need to make energy-efficient decisions to maximize benefits and minimize costs, a tradeoff exemplified in effort expenditure (1-3). A key example occurs during foraging, where an overestimation of effort can lead to inaction and starvation (4), whereas underestimation of effort can result in persistent failure, as exemplified in the myth of Sisyphus (5).In a naturalistic environment, we often simultaneously learn about success in expending sufficient effort into an action as well as the reward we obtain from this same action. The reward outcomes that signal success and failure of an action are usually clear, although the effort necessary to attain success is often less transparent. Only by repeatedly experiencing success and failure is it possible to acquire an estimate of an optimal level of effort needed to succeed, without unnecessary waste of energy. This type of learning is important in contexts as diverse as foraging, hunting, and harvesting (6-8). Hull in his "law of less work" proposed that organisms "gradually learn" how to minimize effort expenditure (9). Surprisingly, we know little regarding the neurocognitive mechanisms that guide this form of simultaneous learning about reward and effort.A mesolimbic dopamine system encodes a teaching signal tethered to prediction of reward outcomes (10, 11). These reward prediction errors (PEs) arise from dopaminergic neurons in substantia nigra and ventral tegmental area (SN/VTA) and are broadcast to ventral striatum (VS) to mediate reward-related adaptation and learning (12, 13). Dopamine is also thought to provide a motivational signal (14-18), while dopaminergic deficits in rodents impair how effort and reward are arbitrated (1, 4, 19). The dorsomedial prefrontal cortex (dmPFC; spanning presupplementary motor area [pre-SMA] and dorsal anterior cingulate cortex [dACC]) is a candidate substrate...

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Section: Discussionmentioning

confidence: 99%

Separate mesocortical and mesolimbic pathways encode effort and reward learning signals

Hauser

Eldar

Dolan

2017

Proc. Natl. Acad. Sci. U.S.A.

120

127

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“…22,32 Stimulation of this region in humans can also elicit feelings of endeavour and "gearing up" for an effortful challenge. 33 The ACC contains CB 1 receptors localized on glutamatergic terminals, which regulate excitatory input into this structure. 34 Thus THC may be dampening presynaptic glutamate release, Average change (%) max thereby decreasing ACC neuron activity.…”

Section: Discussionmentioning

confidence: 99%

Δ9-Tetrahydrocannabinol decreases willingness to exert cognitive effort in male rats

Silveira

Adams

Morena

et al. 2017

JPN

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“…In DLB, apathy, hallucinations, and sleep disorders are some of the most frequently cited treatment-responsive symptoms after treatment with cholinesterase inhibitor drugs (1,34). In addition, the ACC has extensive projections to the amygdala, ventral striatum, and nucleus accumbens, and this circuit is important for goal-directed and motivated behaviors (32,35). Other neuroimaging studies, including PET measures of 18 F-FDG metabolism and structural brain changes on MRI, have also supported the role of ACC in apathy (32,36,37).…”

Section: Discussionmentioning

confidence: 99%

¹²³I-Iodobenzovesamicol SPECT Imaging of Cholinergic Systems in Dementia with Lewy Bodies

et al. 2016

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Cholinergic alterations in dementia with Lewy bodies (DLB) have been widely documented in postmortem studies, whereas in vivo studies are sparse, particularly at the subcortical level. We used 123 I-iodobenzovesamicol, a SPECT radiotracer of the vesicular acetylcholine transporter, to evaluate in vivo in DLB the integrity of the 3 main cholinergic pathways-the Ch1 (septohippocampal), the Ch4 (innominatocortical), and the Ch5 (pontothalamic) cholinergic pathwaysas well as the striatal cholinergic interneurons. In addition, we assessed the involvement of the cholinergic system in cognitive and neuropsychiatric disorders in DLB patients. Methods: Twelve healthy volunteers (median age, 72 y; interquartile range, 6.25 y) and 11 DLB patients (median age, 76 y; interquartile range, 10.50 y) underwent a dynamic 123 I-iodobenzovesamicol SPECT scan and an MRI scan. MR images were automatically segmented, providing the volumes of several regions of interest, including the striatum and cholinergic terminals in Ch1 (hippocampus), Ch4 (cortical lobes), and Ch5 (thalamus). For each region of interest and each subject, pharmacokinetic modeling allowed calculation of the nondisplaceable binding potential (BP ND ) values for the binding of 123 I-iodobenzovesamicol to the vesicular acetylcholine transporter. A neuropsychological evaluation of participants was performed with the Mini-Mental State Examination and the Grober-Buschke, Set, visual discrimination, Benton, and Wechsler tests, and cognitive fluctuations and apathy were also assessed. Results: Compared with BP ND values for healthy subjects, BP ND values for DLB patients were significantly lower in the Ch4 terminal regions of the anterior cingulate cortex and the superior and inferior parietal cortices (P 5 0.0006, 0.0015, and 0.0023, respectively), in the Ch5 terminal region of the thalamus (P 5 0.0003), and in the striatum (P 5 0.0042). All of the neuropsychological test scores were significantly lower in DLB patients than in healthy subjects. Four DLB patients with apathy and 4 DLB patients without apathy were identified. For the anterior cingulate cortex, compared with BP ND values in healthy subjects, BP ND values were significantly lower in patients with apathy (P 5 0.004) and were unchanged in patients without apathy. Conclusion: Our results confirm the existence in DLB of cholinergic alterations, reaching both cortical and subcortical levels, including the Ch5 pathway and the striatum. Alterations in cholinergic transmission in the anterior cingulate cortex could be closely associated with the development of apathy.

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The Will to Persevere Induced by Electrical Stimulation of the Human Cingulate Gyrus

Cited by 208 publications

References 31 publications

Separate mesocortical and mesolimbic pathways encode effort and reward learning signals

Separate mesocortical and mesolimbic pathways encode effort and reward learning signals

Δ9-Tetrahydrocannabinol decreases willingness to exert cognitive effort in male rats

¹²³I-Iodobenzovesamicol SPECT Imaging of Cholinergic Systems in Dementia with Lewy Bodies

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The Will to Persevere Induced by Electrical Stimulation of the Human Cingulate Gyrus

Cited by 208 publications

References 31 publications

Separate mesocortical and mesolimbic pathways encode effort and reward learning signals

Separate mesocortical and mesolimbic pathways encode effort and reward learning signals

Δ9-Tetrahydrocannabinol decreases willingness to exert cognitive effort in male rats

123I-Iodobenzovesamicol SPECT Imaging of Cholinergic Systems in Dementia with Lewy Bodies

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¹²³I-Iodobenzovesamicol SPECT Imaging of Cholinergic Systems in Dementia with Lewy Bodies