Neural basis of motivational approach and withdrawal behaviors in neurodegenerative disease

Shinagawa, Shunichiro; Adhimoolam, Babu; Sturm, Virginia E.; Shany‐Ur, Tal; Ross, Parnian Toofanian; Zackey, Diana; Poorzand, Pardis; Grossman, Sebastian P.; Miller, Bruce L.; Rankin, Katherine P.

doi:10.1002/brb3.350

Cited by 21 publications

(13 citation statements)

References 80 publications

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“…For example, our GM observations suggest that the cingulate may contribute to both initiation and motivation. This is not a surprising finding given the role of the ACC in generating response to punishment cues (Shinagawa et al, 2015 ). Additionally, we observed a significant correlation between initiation and motivation performance ( r = 0.78; p < 0.001).…”

Section: Discussionmentioning

confidence: 71%

Apathy in Frontotemporal Degeneration: Neuroanatomical Evidence of Impaired Goal-directed Behavior

Massimo

Powers

Evans

et al. 2015

Front. Hum. Neurosci.

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Background: Apathy, the major manifestation of impaired goal-directed behavior (GDB), is the most common neuropsychiatric syndrome associated with behavioral variant frontotemporal degeneration (bvFTD). The behavioral and biological mechanisms of apathy, however, are not well understood. We hypothesized that GDB has multiple components—including at least initiation, planning and motivation—and that GDB is supported by a network of multiple frontal brain regions. In this study, we examined this hypothesis by evaluating the selective breakdown of GDB in bvFTD, and relating these deficits to gray matter (GM) atrophy and white matter (WM) integrity.Methods: Eighteen apathetic bvFTD participants and 17 healthy controls completed the Philadelphia Apathy Computerized Test (PACT). This test quantifies each of three components of GDB hypothesized to contribute to apathy. We then used regression analyses to relate PACT scores to GM atrophy and reduced white matter (WM) fractional anisotropy (FA) in bvFTD.Results: Compared to controls, bvFTD participants demonstrated significant impairments in each of the three hypothesized components of GDB that contribute to apathy. Regression analyses related each component to disease in specific GM structures and associated WM tracts. Poor initiation thus was related to GM atrophy in anterior cingulate and reduced FA in the cingulum. Planning impairment was related to GM atrophy in dorsolateral prefrontal cortex and reduced FA in superior longitudinal fasciculus. Poor motivation was related to GM atrophy in orbitofrontal cortex (OFC) and reduced FA in uncinate fasciculus (UNC).Conclusions: bvFTD patients have difficulty with initiation, planning and motivation components of GDB. These findings are consistent with the hypotheses that GDB encompasses at least three processes, that these are supported by a large-scale neural network within specific portions of the frontal lobe, and that degradation of any one of these prefrontal regions in bvFTD may contribute to apathy.

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Section: Discussionmentioning

confidence: 71%

Apathy in Frontotemporal Degeneration: Neuroanatomical Evidence of Impaired Goal-directed Behavior

Massimo

Powers

Evans

et al. 2015

Front. Hum. Neurosci.

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“…The left dorsal anterior insula/ opercular region responds preferentially to unpleasant compared to pleasant tastes (Small et al, 2003), suggesting that a lesion to this area would selectively impair response to the unpleasant. Integrity of regions including left insula/ operculum correlates with an intact Behavioural Inhibition Scale (BIS) score, a marker of responsiveness to punishment, in bvFTD and Alzheimer's disease (Shinagawa et al, 2015). These findings suggest a role of this left insula region in processing aversive information, and that degeneration of this area leads to insensitivity to the negative or excessive display of the positive.…”

Section: Discussionmentioning

confidence: 87%

Reward deficits in behavioural variant frontotemporal dementia include insensitivity to negative stimuli

Perry

Datta

Sturm

et al. 2017

Brain

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During reward processing individuals weigh positive and negative features of a stimulus to determine whether they will pursue or avoid it. Though patients with behavioural variant frontotemporal dementia display changes in their pursuit of rewards, such as food, alcohol, money, and sex, the basis for these shifts is not clearly established. In particular, it is unknown whether patients' behaviour results from excessive focus on rewards, insensitivity to punishment, or to dysfunction in a particular stage of reward processing, such as anticipation, consumption, or action selection. Our goal was to determine the nature of the reward deficit in behavioural variant frontotemporal dementia and its underlying anatomy. We devised a series of tasks involving pleasant, unpleasant, and neutral olfactory stimuli, designed to separate distinct phases of reward processing. In a group of 25 patients with behavioural variant frontotemporal dementia and 21 control subjects, diagnosis by valence interactions revealed that patients with behavioural variant frontotemporal dementia rated unpleasant odours as less aversive than did controls and displayed lower skin conductance responses when anticipating an upcoming aversive odour. Subjective pleasantness ratings and skin conductance responses did not differ between behavioural variant frontotemporal dementia and controls for pleasant or neutral smells. In a task designed to measure the effort subjects would expend to smell or avoid smelling a stimulus, patients with behavioural variant frontotemporal dementia were less motivated, and therefore less successful than control subjects, at avoiding what they preferred not to smell, but had equivalent success at obtaining stimuli they found rewarding. Voxel-based morphometry of patients with behavioural variant frontotemporal dementia revealed that the inability to subjectively differentiate the valence of pleasant and unpleasant odours correlated with atrophy in right ventral mid-insula and right amygdala. High pleasantness ratings of unpleasant stimuli correlated with left dorsal anterior insula and frontal pole atrophy. These findings indicate that insensitivity to negative information may be a key component of the reward-seeking behaviours in behavioural variant frontotemporal dementia, and may relate to degeneration of structures that are involved in representing the emotional salience of sensory information.

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“…Increased levels of avoidance motivation is one of the most important traits in depression ( Spielberg, 2011 ). Investigators found a positive correlation between the volume of both the precentral gyrus and the anterior cingulate cortex with higher levels of anxiety and the corresponding avoidant motivational set in neurodegenerative disease ( Shinagawa et al, 2015 ). We speculate that the decreased precentral VBM may be associated with avoidance motivation in MDD and StD.…”

Section: Discussionmentioning

confidence: 99%

Anatomical brain difference of subthreshold depression in young and middle-aged individuals

Wang

Hwang

et al. 2017

NeuroImage: Clinical

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BackgroundSubthreshold depression (StD) is associated with substantial functional impairments due to depressive symptoms that do not fully meet the diagnosis of major depressive disorder (MDD). Its high incidence in the general population and debilitating symptoms has recently put it at the forefront of mood disorder research.AimIn this study we investigated common volumetric brain changes in both young and middle-aged StD patients.MethodsTwo cohorts of StD patients, young and middle-aged, (n = 57) and matched controls (n = 76) underwent voxel-based morphometry (VBM).ResultsVBM analysis found that: 1) compared with healthy controls, StD patients showed decreased gray matter volume (GMV) in the bilateral globus pallidus and precentral gyrus, as well as increased GMV in the left thalamus and right rostral anterior cingulate cortex/medial prefrontal cortex; 2) there is a significant association between Center for Epidemiological Studies Depression Scale scores and the bilateral globus pallidus (negative) and left thalamus (positive); 3) there is no interaction between age (young vs. middle-age) and group (StD vs. controls).ConclusionsOur findings indicate significant VBM brain changes in both young and middle-aged individuals with StD. Individuals with StD, regardless of age, may share common neural characteristics.

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Neural basis of motivational approach and withdrawal behaviors in neurodegenerative disease

Cited by 21 publications

References 80 publications

Apathy in Frontotemporal Degeneration: Neuroanatomical Evidence of Impaired Goal-directed Behavior

Apathy in Frontotemporal Degeneration: Neuroanatomical Evidence of Impaired Goal-directed Behavior

Reward deficits in behavioural variant frontotemporal dementia include insensitivity to negative stimuli

Anatomical brain difference of subthreshold depression in young and middle-aged individuals

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