Reward Dependent Invigoration Relates to Theta Oscillations and Is Predicted by Dopaminergic Midbrain Integrity in Healthy Elderly

Motivation can have invigorating effects on behavior via dopaminergic neuromodulation. While this relationship has mainly been established in theoretical models and studies in younger subjects, the impact of structural declines of the dopaminergic system during healthy aging remains unclear. To investigate this issue, we used electroencephalography (EEG) in healthy young and elderly humans in a reward-learning paradigm. Specifically, scene images were initially encoded by combining them with cues predicting monetary reward (high vs. low reward). Subsequently, recognition memory for the scenes was tested. As a main finding, we can show that response times (RTs) during encoding were faster for high reward predicting images in the young but not elderly participants. This pattern was resembled in power changes in the theta-band (4–7 Hz). Importantly, analyses of structural MRI data revealed that individual reward-related differences in the elderlies’ response time could be predicted by the structural integrity of the dopaminergic substantia nigra (SN; as measured by magnetization transfer (MT)). These findings suggest a close relationship between reward-based invigoration, theta oscillations and age-dependent changes of the dopaminergic system.

[1]  Hans-Jochen Heinze,et al.  A close relationship between verbal memory and SN/VTA integrity in young and older adults , 2008, Neuropsychologia.

[2]  P. J. Basser,et al.  Role of myelin plasticity in oscillations and synchrony of neuronal activity , 2014, Neuroscience.

[3]  A. Peters The effects of normal aging on myelin and nerve fibers: A review , 2002, Journal of neurocytology.

[4]  J. Krakauer,et al.  Why Don't We Move Faster? Parkinson's Disease, Movement Vigor, and Implicit Motivation , 2007, The Journal of Neuroscience.

[5]  J. Lisman,et al.  The Hippocampal-VTA Loop: Controlling the Entry of Information into Long-Term Memory , 2005, Neuron.

[6]  Rony Paz,et al.  Theta synchronizes the activity of medial prefrontal neurons during learning. , 2008, Learning & memory.

[7]  N. Lavie,et al.  The influence of perceptual load on age differences in selective attention. , 1998, Psychology and aging.

[8]  Trevor W. Robbins,et al.  Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi on performance of a 5-choice serial reaction time task in rats: Implications for theories of selective attention and arousal , 1989, Behavioural Brain Research.

[9]  Gregory R. Samanez-Larkin,et al.  Anticipation of monetary gain but not loss in healthy older adults , 2007, Nature Neuroscience.

[10]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[11]  W. Schultz,et al.  Adaptive Coding of Reward Value by Dopamine Neurons , 2005, Science.

[12]  Klaus-Armin Nave,et al.  Myelination of the nervous system: mechanisms and functions. , 2014, Annual review of cell and developmental biology.

[13]  Richard S. Frackowiak,et al.  Disentangling in vivo the effects of iron content and atrophy on the ageing human brain , 2014, NeuroImage.

[14]  R. Dolan,et al.  Contextual Novelty Modulates the Neural Dynamics of Reward Anticipation , 2011, The Journal of Neuroscience.

[15]  Nora A. Herweg,et al.  Theta-Alpha Oscillations Bind the Hippocampus, Prefrontal Cortex, and Striatum during Recollection: Evidence from Simultaneous EEG–fMRI , 2016, The Journal of Neuroscience.

[16]  H. Heinze,et al.  Reward-Related fMRI Activation of Dopaminergic Midbrain Is Associated with Enhanced Hippocampus- Dependent Long-Term Memory Formation , 2005, Neuron.

[17]  H. Groenewegen,et al.  The nucleus accumbens: gateway for limbic structures to reach the motor system? , 1996, Progress in brain research.

[18]  G. Bartzokis Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease , 2004, Neurobiology of Aging.

[19]  L. Nyberg,et al.  The correlative triad among aging, dopamine, and cognition: Current status and future prospects , 2006, Neuroscience & Biobehavioral Reviews.

[20]  Joshua M. Carlson,et al.  Midbrain volume predicts fMRI and ERP measures of reward reactivity , 2014, Brain Structure and Function.

[21]  T. Womelsdorf,et al.  Human Neuroscience , 2022 .

[22]  A. Lees,et al.  Ageing and Parkinson's disease: substantia nigra regional selectivity. , 1991, Brain : a journal of neurology.

[23]  Ulrik R Beierholm,et al.  Dopamine Modulates Reward-Related Vigor , 2013, Neuropsychopharmacology.

[24]  Y. Niv Cost, Benefit, Tonic, Phasic , 2007, Annals of the New York Academy of Sciences.

[25]  Peter Dayan,et al.  Vigor in the Face of Fluctuating Rates of Reward: An Experimental Examination , 2011, Journal of Cognitive Neuroscience.

[26]  Hans-Jochen Heinze,et al.  Mesolimbic novelty processing in older adults. , 2007, Cerebral cortex.

[27]  Viktor Müller,et al.  Life Span Differences in Electrophysiological Correlates of Monitoring Gains and Losses during Probabilistic Reinforcement Learning , 2011, Journal of Cognitive Neuroscience.

[28]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .

[29]  Emrah Duzel,et al.  A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP , 2011, Trends in Neurosciences.

[30]  H. Heinze,et al.  Ageing and early-stage Parkinson's disease affect separable neural mechanisms of mesolimbic reward processing. , 2007, Brain : a journal of neurology.

[31]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[32]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[33]  Brian Knutson,et al.  Dissociation of reward anticipation and outcome with event-related fMRI , 2001, Neuroreport.

[34]  L. Colgin Rhythms of the hippocampal network , 2016, Nature Reviews Neuroscience.

[35]  N. Burgess,et al.  Brain oscillations and memory , 2010, Current Opinion in Neurobiology.

[36]  Vincent B. McGinty,et al.  Invigoration of Reward Seeking by Cue and Proximity Encoding in the Nucleus Accumbens , 2013, Neuron.

[37]  Arne D. Ekstrom,et al.  Prestimulus theta activity predicts correct source memory retrieval , 2011, Proceedings of the National Academy of Sciences.

[38]  M. Vinck,et al.  Theta-Band Phase Locking of Orbitofrontal Neurons during Reward Expectancy , 2010, The Journal of Neuroscience.

[39]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[40]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[41]  Mark W. Woolrich,et al.  FSL , 2012, NeuroImage.

[42]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[43]  S. Haber,et al.  The Reward Circuit: Linking Primate Anatomy and Human Imaging , 2010, Neuropsychopharmacology.

[44]  Nico Bunzeck,et al.  Contextual interaction between novelty and reward processing within the mesolimbic system , 2011, Human brain mapping.

[45]  Darrell A. Worthy,et al.  Adult age differences in frontostriatal representation of prediction error but not reward outcome , 2014, Cognitive, affective & behavioral neuroscience.

[46]  David H. Miller,et al.  Magnetization transfer ratio and myelin in postmortem multiple sclerosis brain , 2004, Annals of neurology.

[47]  C. Rorden,et al.  Stereotaxic display of brain lesions. , 2000, Behavioural neurology.

[48]  Thomas H. B. FitzGerald,et al.  Widespread age-related differences in the human brain microstructure revealed by quantitative magnetic resonance imaging , 2014, Neurobiology of Aging.

[49]  H. Heinze,et al.  Mesolimbic Functional Magnetic Resonance Imaging Activations during Reward Anticipation Correlate with Reward-Related Ventral Striatal Dopamine Release , 2008, The Journal of Neuroscience.

[50]  J. Fell,et al.  Memory formation by neuronal synchronization , 2006, Brain Research Reviews.

[51]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

[52]  Nico Bunzeck,et al.  Dopaminergic stimulation facilitates working memory and differentially affects prefrontal low theta oscillations , 2014, NeuroImage.

[53]  Richard S. Frackowiak,et al.  Improved segmentation of deep brain grey matter structures using magnetization transfer (MT) parameter maps , 2009, NeuroImage.

[54]  Nico Bunzeck,et al.  Acetylcholine modulates human working memory and subsequent familiarity based recognition via alpha oscillations , 2016, NeuroImage.

[55]  W. Schultz,et al.  Discrete Coding of Reward Probability and Uncertainty by Dopamine Neurons , 2003, Science.

[56]  Arne D. Ekstrom,et al.  Expected reward modulates encoding-related theta activity before an event , 2013, NeuroImage.

[57]  N Butters,et al.  Detection of abnormal memory decline in mild cases of Alzheimer's disease using CERAD neuropsychological measures. , 1991, Archives of neurology.

[58]  R. Gur,et al.  Effects of antipsychotic treatment on cognition in healthy subjects , 2013, Journal of psychopharmacology.

[59]  Brian Knutson,et al.  Reward-Motivated Learning: Mesolimbic Activation Precedes Memory Formation , 2006, Neuron.

[60]  G. Remington,et al.  Impact of haloperidol, a dopamine D2 antagonist, on cognition and mood , 2006, Schizophrenia Research.

[61]  Nikolaus Weiskopf,et al.  Iron Level and Myelin Content in the Ventral Striatum Predict Memory Performance in the Aging Brain , 2016, The Journal of Neuroscience.

[62]  Massimo Silvetti,et al.  Reward expectation and prediction error in human medial frontal cortex: An EEG study , 2014, NeuroImage.

[63]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[64]  Tatsuo K Sato,et al.  Correlated Coding of Motivation and Outcome of Decision by Dopamine Neurons , 2003, The Journal of Neuroscience.

[65]  P. Dayan Instrumental vigour in punishment and reward , 2012, The European journal of neuroscience.

[66]  M. J. Wanat,et al.  Phasic Dopamine Transmission Reflects Initiation Vigor and Exerted Effort in an Action- and Region-Specific Manner , 2016, The Journal of Neuroscience.

[67]  Richard S. Frackowiak,et al.  Regional specificity of MRI contrast parameter changes in normal ageing revealed by voxel-based quantification (VBQ) , 2011, NeuroImage.

[68]  J. Yesavage,et al.  Proposed Factor Structure of the Geriatric Depression Scale , 1991, International Psychogeriatrics.

[69]  R. Dolan,et al.  How the Brain Translates Money into Force: A Neuroimaging Study of Subliminal Motivation , 2007, Science.

[70]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[71]  P. Dechent,et al.  High‐resolution maps of magnetization transfer with inherent correction for RF inhomogeneity and T1 relaxation obtained from 3D FLASH MRI , 2008, Magnetic resonance in medicine.