Abstract
A recent virtual-lesion study using inhibitory repetitive transcranial magnetic stimulation (rTMS) confirmed the causal behavioral relevance of the precuneus in the evaluation of one’s own memory performance (aka mnemonic metacognition). This study’s goal is to elucidate how these TMS-induced neuromodulatory effects might relate to the neural correlates and be modulated by individual anatomical profiles in relation to meta-memory. In a within-subjects design, we assessed the impact of 20-min rTMS over the precuneus, compared to the vertex, across three magnetic resonance imaging (MRI) neuro-profiles on 18 healthy subjects during a memory versus a perceptual task. Task-based functional MRI revealed that BOLD signal magnitude in the precuneus is associated with variation in individual meta-memory efficiency. Moreover, individuals with higher resting-state functional connectivity (rs-fcMRI) between the precuneus and the hippocampus, or smaller gray matter volume in the stimulated precuneal region exhibit considerably higher vulnerability to the TMS effect. These effects were not observed in the perceptual domain. Thus, we provide compelling evidence in outlining a possible circuit encompassing the precuneus and its mnemonic midbrain neighbor the hippocampus at the service of realizing our meta-awareness during memory recollection of episodic details.
Highlights
-
TMS disrupts the correlation between BOLD activity and meta-memory ability.
-
TMS effect is modulated by rs-fcMRI between precuneus and hippocampus.
-
Individuals with greater precuneal gray matter volume more immune to TMS effect.
This is a preview of subscription content, access via your institution.
References
Allen M et al (2017) Metacognitive ability correlates with hippocampal and prefrontal microstructure. Neuroimage 149:415–423. https://doi.org/10.1016/j.neuroimage.2017.02.008
Ashburner J (2007) A fast diffeomorphic image registration algorithm. Neuroimage 38:95–113. https://doi.org/10.1016/j.neuroimage.2007.07.007
Baird B, Smallwood J, Gorgolewski KJ, Margulies DS (2013) Medial and lateral networks in anterior prefrontal cortex support metacognitive ability for memory and perception. J Neurosci 33:16657–16665. https://doi.org/10.1523/JNEUROSCI.0786-13.2013
Bonni S, Veniero D, Mastropasqua C, Ponzo V, Caltagirone C, Bozzali M, Koch G (2015) TMS evidence for a selective role of the precuneus in source memory retrieval. Behav Brain Res 282:70–75. https://doi.org/10.1016/j.bbr.2014.12.032
Chen R, Seitz RJ (2001) Changing cortical excitability with low-frequency magnetic stimulation. Neurology 57:379–380
Chua EF, Schacter DL, Rand-Giovannetti E, Sperling RA (2006) Understanding metamemory: neural correlates of the cognitive process and subjective level of confidence in recognition memory. Neuroimage 29:1150–1160. https://doi.org/10.1016/j.neuroimage.2005.09.058
Ciaramelli E, Faggi G, Scarpazza C, Mattioli F, Spaniol J, Ghetti S, Moscovitch M (2017) Subjective recollection independent from multifeatural context retrieval following damage to the posterior parietal cortex. Cortex 91:114–125. https://doi.org/10.1016/j.cortex.2017.03.015
Daitch AL, Parvizi J (2018) Spatial and temporal heterogeneity of neural responses in human posteromedial cortex. Proc Natl Acad Sci USA 1:1. https://doi.org/10.1073/pnas.1721714115
Davachi L, DuBrow S (2015) How the hippocampus preserves order: the role of prediction and context. Trends Cognit Sci 19:92–99. https://doi.org/10.1016/j.tics.2014.12.004
Esteban O et al (2019) fMRIPrep: a robust preprocessing pipeline for functional. MRI Nat Methods 16:111–116. https://doi.org/10.1038/s41592-018-0235-4
Fleming SM, Lau HC (2014) How to measure metacognition. Front Hum Neurosci 8:443. https://doi.org/10.3389/fnhum.2014.00443
Fleming SM, Weil RS, Nagy Z, Dolan RJ, Rees G (2010) Relating introspective accuracy to individual differences in brain structure. Science 329:1541–1543. https://doi.org/10.1126/science.1191883
Fleming SM, Huijgen J, Dolan RJ (2012) Prefrontal contributions to metacognition in perceptual decision making. J Neurosci 32:6117–6125. https://doi.org/10.1523/JNEUROSCI.6489-11.2012
Fleming SM, Ryu J, Golfinos JG, Blackmon KE (2014) Domain-specific impairment in metacognitive accuracy following anterior prefrontal lesions. Brain 137:2811–2822. https://doi.org/10.1093/brain/awu221
Gorgolewski K, Burns CD, Madison C, Clark D, Halchenko YO, Waskom ML, Ghosh SS (2011) Nipype: a flexible, lightweight and extensible neuroimaging data processing framework in python. Front Neuroinform 5:13. https://doi.org/10.3389/fninf.2011.00013
Hebart MN, Schriever Y, Donner TH, Haynes JD (2016) The relationship between perceptual decision variables and confidence in the human brain. Cereb Cortex 26:118–130. https://doi.org/10.1093/cercor/bhu181
Heereman J, Walter H, Heekeren HR (2015) A task-independent neural representation of subjective certainty in visual perception. Front Hum Neurosci 9:551. https://doi.org/10.3389/fnhum.2015.00551
Iyer MB, Schleper N, Wassermann EM (2003) Priming stimulation enhances the depressant effect of low-frequency repetitive transcranial magnetic stimulation. J Neurosci 23:10867–10872
Jung J, Bungert A, Bowtell R, Jackson SR (2016) Vertex stimulation as a control site for transcranial magnetic stimulation: a concurrent TMS/fMRI study. Brain Stimul 9:58–64. https://doi.org/10.1016/j.brs.2015.09.008
Kepecs A, Uchida N, Zariwala HA, Mainen ZF (2008) Neural correlates, computation and behavioural impact of decision confidence. Nature 455:227–231. https://doi.org/10.1038/nature07200
Kim J, Kim YH, Lee JH (2013) Hippocampus-precuneus functional connectivity as an early sign of Alzheimer’s disease: a preliminary study using structural and functional magnetic resonance imaging data. Brain Res 1495:18–29. https://doi.org/10.1016/j.brainres.2012.12.011
Koch G et al (2018) Transcranial magnetic stimulation of the precuneus enhances memory and neural activity in prodromal Alzheimer’s disease. Neuroimage 169:302–311. https://doi.org/10.1016/j.neuroimage.2017.12.048
Kraft A et al (2015) TMS over the right precuneus reduces the bilateral field advantage in visual short term memory capacity. Brain Stimul 8:216–223. https://doi.org/10.1016/j.brs.2014.11.004
Kwok SC, Shallice T, Macaluso E (2012) Functional anatomy of temporal organisation and domain-specificity of episodic memory retrieval. Neuropsychologia 50:2943–2955. https://doi.org/10.1016/j.neuropsychologia.2012.07.025
Maniscalco B, Lau H (2012) A signal detection theoretic approach for estimating metacognitive sensitivity from confidence ratings. Conscious Cognit 21:422–430. https://doi.org/10.1016/j.concog.2011.09.021
Margulies DS et al (2009) Precuneus shares intrinsic functional architecture in humans and monkeys. Proc Natl Acad Sci USA 106:20069–20074. https://doi.org/10.1073/pnas.0905314106
McCurdy LY, Maniscalco B, Metcalfe J, Liu KY, de Lange FP, Lau H (2013) Anatomical coupling between distinct metacognitive systems for memory and visual perception. J Neurosci 33:1897–1906. https://doi.org/10.1523/JNEUROSCI.1890-12.2013
Middlebrooks PG, Sommer MA (2012) Neuronal correlates of metacognition in primate frontal cortex. Neuron 75:517–530. https://doi.org/10.1016/j.neuron.2012.05.028
Miyamoto K, Osada T, Setsuie R, Takeda M, Tamura K, Adachi Y, Miyashita Y (2017) Causal neural network of metamemory for retrospection in primates. Science 355:188–193. https://doi.org/10.1126/science.aal0162
Miyamoto K, Setsuie R, Osada T, Miyashita Y (2018) Reversible silencing of the frontopolar cortex selectively impairs metacognitive judgment on non-experience in primates. Neuron 97(980–989):e986. https://doi.org/10.1016/j.neuron.2017.12.040
Morales J, Lau H, Fleming SM (2018) Domain-general and domain-specific patterns of activity supporting metacognition in human prefrontal cortex. J Neurosci 38:3534–3546. https://doi.org/10.1523/JNEUROSCI.2360-17.2018
Pruim RHR, Mennes M, van Rooij D, Llera A, Buitelaar JK, Beckmann CF (2015) ICA-AROMA: a robust ICA-based strategy for removing motion artifacts from fMRI data. Neuroimage 112:267–277. https://doi.org/10.1016/j.neuroimage.2015.02.064
Qiu L, Su J, Ni Y, Bai Y, Zhang X, Li X, Wan X (2018) The neural system of metacognition accompanying decision-making in the prefrontal cortex. PLoS Biol 16:e2004037. https://doi.org/10.1371/journal.pbio.2004037
Ren Y et al (2018) Effective connectivity of the anterior hippocampus predicts recollection confidence during natural memory retrieval. Nat Commun 9:4875. https://doi.org/10.1038/s41467-018-07325-4
Rossini PM et al (2015) Non-invasive electrical and magnetic stimulation of the brain, spinal cord, roots and peripheral nerves: basic principles and procedures for routine clinical and research application. An updated report from an IFCN committee. Clin Neurophysiol 126:1071–1107. https://doi.org/10.1016/j.clinph.2015.02.001
Rounis E, Maniscalco B, Rothwell JC, Passingham RE, Lau H (2010) Theta-burst transcranial magnetic stimulation to the prefrontal cortex impairs metacognitive visual awareness. Cognit Neurosci 1:165–175. https://doi.org/10.1080/17588921003632529
Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52:1059–1069. https://doi.org/10.1016/j.neuroimage.2009.10.003
Rutishauser U, Aflalo T, Rosario ER, Pouratian N, Andersen RA (2018) Single-neuron representation of memory strength and recognition confidence in left human posterior parietal cortex. Neuron 97:209–220. https://doi.org/10.1016/j.neuron.2017.11.029(e203)
Shekhar M, Rahnev D (2018) Distinguishing the roles of dorsolateral and anterior PFC in visual metacognition. J Neurosci 38:5078–5087. https://doi.org/10.1523/JNEUROSCI.3484-17.2018
Simons JS, Peers PV, Mazuz YS, Berryhill ME, Olson IR (2010) Dissociation between memory accuracy and memory confidence following bilateral parietal lesions. Cereb Cortex 20:479–485. https://doi.org/10.1093/cercor/bhp116
Talairach J, Tournoux P (1988) Co-planar stereotaxic atlas of the human brain. Thieme, New York
Tustison NJ, Avants BB, Cook PA, Zheng Y, Egan A, Yushkevich PA, Gee JC (2010) N4ITK: improved N3 bias correction. IEEE Trans Med Imaging 29:1310–1320. https://doi.org/10.1109/TMI.2010.2046908
Vaccaro AG, Fleming SM (2018) Thinking about thinking: a coordinate-based meta-analysis of neuroimaging studies of metacognitive judgements. Brain Neurosci Adv 2:2398212818810591. https://doi.org/10.1177/2398212818810591
Vincent JL, Snyder AZ, Fox MD, Shannon BJ, Andrews JR, Raichle ME, Buckner RL (2006) Coherent spontaneous activity identifies a hippocampal-parietal memory network. J Neurophysiol 96:3517–3531. https://doi.org/10.1152/jn.00048.2006
Vul E, Pashler H (2017) Suspiciously high correlations in brain imaging research. In: Lilienfeld SO, Waldman ID (eds) Psychological science under scrutiny: recent challenges and proposed solutions. Wiley, pp 196–220
Vul E, Harris C, Winkielman P, Pashler H (2009) Puzzlingly high correlations in fMRI studies of emotion, personality, and social cognition. Perspect psychol sci 4:274–290
Wagner AD, Shannon BJ, Kahn I, Buckner RL (2005) Parietal lobe contributions to episodic memory retrieval. Trends Cognit Sci 9:445–453. https://doi.org/10.1016/j.tics.2005.07.001
Wang JX et al (2014) Targeted enhancement of cortical-hippocampal brain networks and associative memory. Science 345:1054–1057. https://doi.org/10.1126/science.1252900
Yarkoni T (2009) Big correlations in little studies: inflated fMRI correlations reflect low statistical power—commentary on Vul et al.(2009). Perspect Psychol Sci 4:294–298
Yazar Y, Bergstrom ZM, Simons JS (2017) Reduced multimodal integration of memory features following continuous theta burst stimulation of angular gyrus. Brain Stimul 10:624–629. https://doi.org/10.1016/j.brs.2017.02.011
Ye Q, Zou F, Lau H, Hu Y, Kwok SC (2018) Causal evidence for mnemonic metacognition in human precuneus. J Neurosci 38:6379–6387. https://doi.org/10.1523/JNEUROSCI.0660-18.2018
Acknowledgements
We thank Elena Makovac for her advice on implementing VBM analysis.
Funding
This work was supported by Ministry of Education of PRC Humanities and Social Sciences Research grant 16YJC190006, STCSM Natural Science Foundation of Shanghai 16ZR1410200, Fundamental Research Funds for the Central Universities 2018ECNU-HWFW007, NYU Shanghai and NYU-ECNU Institute of Brain and Cognitive Science at NYU Shanghai (S.C.K.); National Institute of Neurological Disorders and Stroke of the National Institutes of Health grant R01NS088628 (H.L.); National Natural Science Foundation of China 31872783 (Y.H.).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
None of the authors has any conflicts of interest to declare.
Ethical approval
All procedures performed in this study involving human participants have been approved by the local ethics committee of the institute (University Committee on Human Research Protection of East China Normal University, UCHRP-ECNU) and are in agreement with the 1964 Helsinki declaration and its later amendments.
Informed consent
All participants gave their informed consent to participate in the study.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ye, Q., Zou, F., Dayan, M. et al. Individual susceptibility to TMS affirms the precuneal role in meta-memory upon recollection. Brain Struct Funct 224, 2407–2419 (2019). https://doi.org/10.1007/s00429-019-01909-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00429-019-01909-6