Hippocampal-targeted Theta-burst Stimulation Enhances Associative Memory Formation

Arielle Tambini, Derek Evan Nee, Mark D'Esposito, Arielle Tambini, Derek Evan Nee, Mark D'Esposito

Abstract

The hippocampus plays a critical role in episodic memory, among other cognitive functions. However, few tools exist to causally manipulate hippocampal function in healthy human participants. Recent work has targeted hippocampal-cortical networks by performing TMS to a region interconnected with the hippocampus, posterior inferior parietal cortex (pIPC). Such hippocampal-targeted TMS enhances associative memory and influences hippocampal functional connectivity. However, it is currently unknown which stages of mnemonic processing (encoding or retrieval) are affected by hippocampal-targeted TMS. Here, we examined whether hippocampal-targeted TMS influences the initial encoding of associations (vs. items) into memory. To selectively influence encoding and not retrieval, we performed continuous theta-burst TMS before participants encoded object-location associations and assessed memory after the direct effect of stimulation dissipated. Relative to control TMS and baseline memory, pIPC TMS enhanced associative memory success and confidence. Item memory was unaffected, demonstrating a selective influence on associative versus item memory. The strength of hippocampal-pIPC functional connectivity predicted TMS-related memory benefits, which was mediated by parahippocampal and retrosplenial cortices. Our findings indicate that hippocampal-targeted TMS can specifically modulate the encoding of new associations into memory without directly influencing retrieval processes and suggest that the ability to influence associative memory may be related to the fidelity of hippocampal TMS targeting. These results support the notion that pIPC TMS may serve as a potential tool for manipulating hippocampal function in healthy participants. Nonetheless, future work combining hippocampal-targeted continuous theta-burst TMS with neuroimaging is needed to better understand the neural basis of TMS-induced memory changes.

Figures

Figure 1.
Figure 1.
TMS targeting and experimental design. (A) A group level map of hippocampal functional connectivity (center) was created using the right middle hippocampus as a seed region (left) from the fMRI study. The connectivity map is overlaid on regions of the angular gyrus defined based on cytoarchitectonic features, posterior PG (PGp, in blue) and anterior PG (PGa, in green; Caspers et al., 2010). A group level ROI (15-mm radius) was created around the location of peak hippocampal connectivity in pIPC. To define hippocampal-targeted pIPC TMS sites (right), participant-specific hippocampal functional connectivity maps were created (red correlation map) and overlaid on the group level ROI (transformed into each participant’s native space; orange shaded region). The TMS site was chosen as the location of each participant’s maximal hippocampal functional connectivity within the group level ROI. All group level maps are available on neurovault.org (neurovault.org/collections/AELKYBHZ/). (B) TMS sites displayed for all participants as spheres (pIPC in blue; control in black). (C) The TMS study consisted of three sessions across 3 consecutive weeks (in addition to a baseline MRI/TMS session). Each week comprised encoding and retrieval sessions, separated by 2–5 hr. During encoding, participants intentionally encoded unique objects and their associated spatial locations and performed an unrelated color discrimination task during the ITI. During retrieval, participants performed a remember/know/new decision for each object, then placed objects labeled as old in their associated spatial location, and rated the confidence of their placement. Behavioral sessions were performed during the baseline (first) session (left). cTBS was performed immediately before encoding during subsequent sessions to either pIPC or the control site (right), with the order of TMS sites counterbalanced across participants. (D) Object placement was modeled as a mixture of memory success (represented as a Gaussian distribution around each object’s location during encoding) and guessing behavior (represented as a uniform distribution across the screen), with the probability of memory success representing the proportion of trials belonging to the memory success distribution.
Figure 2.
Figure 2.
Associative and item memory across sessions. (A) Associative (object–location) memory for each session (baseline memory testing, pIPC TMS, and control TMS). The probability of object-location memory success is shown in the left plot, and the proportion of high and medium confident trials is shown in the right plot. (B) Item (object) memory for each session. Left bars show the proportion of item hits, and right bars show corrected item memory (proportion of hits minus false alarms). (C) Between-session changes in associative memory (probability of object-location memory success; dark green) and corrected item memory (light green). All error bars show standard deviation of the mean across participants, and individual circles correspond to data points for individual participants. *p < .05.
Figure 3.
Figure 3.
Individual differences in memory changes across TMS sessions. TMS-related changes in associative (object–location) memory success were correlated with changes in recollection as a function of hippocampal-targeted TMS (pIPC minus control TMS; left plot) across participants. Differences in familiarity based on TMS site were not reliably related to changes in associative memory success (right plot). Robust regression was used to assess all across-participant correlations.
Figure 4.
Figure 4.
Intrinsic levels of hippocampal–pIPC functional connectivity, TMS-related benefits in associative memory, and potential mediators of hippocampal–pIPC functional connectivity. (A) Intrinsic functional connectivity between the hippocampus and pIPC TMS site was related to changes in the probability of associative memory success for pIPC versus control TMS. (B) Functional connectivity between the hippocampus and the control TMS site was not related to changes in associative memory success between TMS sites. (C) The strongest mediators of hippocampal–pIPC functional connectivity were identified from the fMRI study (excluding overlapping participants with the TMS study) and included RSC (left) and PHC (right). The statistical map is available on neurovault.org. (D) Intrinsic hippocampal–pIPC functional connectivity no longer predicted TMS-related benefits in associative memory success when controlling for the BOLD signal in right PHC. This relationship was significantly weaker than the correlation in A.

References

    1. Andersen RA, Asanuma C, Essick G, & Siegel RM (1990). Corticocortical connections of anatomically and physiologically defined subdivisions within the inferior parietal lobe. Journal of Comparative Neurology, 296, 65–113.
    1. Andoh J, & Zatorre RJ (2013). Mapping interhemispheric connectivity using functional MRI after transcranial magnetic stimulation on the human auditory cortex. Neuroimage, 79, 162–171.
    1. Andrews-Hanna JR, Reidler JS, Huang C, & Buckner RL (2010). Evidence for the default network’s role in spontaneous cognition. Journal of Neurophysiology, 104, 322–335.
    1. Andrews-Hanna JR, Reidler JS, Sepulcre J, Poulin R, & Buckner RL (2010). Functional–anatomic fractionation of the brain’s default network. Neuron, 65, 550–562.
    1. Andrews-Hanna JR, Smallwood J, & Spreng RN (2014). The default network and self-generated thought: Component processes, dynamic control, and clinical relevance. Annals of the New York Academy of Sciences, 1316, 29–52.
    1. Avants BB, Epstein CL, Grossman M, & Gee JC (2008). Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain. Medical Image Analysis, 12, 26–41.
    1. Baumann O, Chan E, & Mattingley JB (2010). Dissociable neural circuits for encoding and retrieval of object locations during active navigation in humans. Neuroimage, 49, 2816–2825.
    1. Baxendale SA, Thompson PJ, & Van Paesschen W (1998). A test of spatial memory and its clinical utility in the pre-surgical investigation of temporal lobe epilepsy patients. Neuropsychologia, 36, 591–602.
    1. Behzadi Y, Restom K, Liau J, & Liu TT (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. Neuroimage, 37, 90–101.
    1. Bohbot VD, Kalina M, Stepankova K, Spackova N, Petrides M, & Nadel L (1998). Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia, 36, 1217–1238.
    1. Buckner RL, Andrews-Hanna JR, & Schacter DL (2008). The brain’s default network: Anatomy, function, and relevance to disease. Annals of the New York Academy of Sciences, 1124, 1–38.
    1. Button KS, Ioannidis JPA, Mokrysz C, Nosek BA, Flint J, Robinson ESJ, et al. (2013). Power failure: Why small sample size undermines the reliability of neuroscience. Nature Reviews Neuroscience, 14, 365–376.
    1. Cameron IGM, Riddle JM, & D’Esposito M (2015). Dissociable roles of dorsolateral prefrontal cortex and frontal eye fields during saccadic eye movements. Frontiers in Human Neuroscience, 9, 613.
    1. Cansino S, Maquet P, Dolan RJ, & Rugg MD (2002). Brain activity underlying encoding and retrieval of source memory. Cerebral Cortex, 12, 1048–1056.
    1. Capotosto P, Babiloni C, Romani GL, & Corbetta M (2014). Resting-state modulation of alpha rhythms by interference with angular gyrus activity. Journal of Cognitive Neuroscience, 26, 107–119.
    1. Cavada C, & Goldman-Rakic PS (1989). Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections. Journal of Comparative Neurology, 287, 393–421.
    1. Chai XJ, Castañón AN, Ongür D, & Whitfield-Gabrieli S (2012). Anticorrelations in resting state networks without global signal regression. Neuroimage, 59, 1420–1428.
    1. Chen AC, & Etkin A (2013). Hippocampal network connectivity and activation differentiates post-traumatic stress disorder from generalized anxiety disorder. Neuropsychopharmacology, 38, 1889–1898.
    1. Cho SS, & Strafella AP (2009). rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS One, 4, e6725.
    1. Christoff K, Gordon AM, Smallwood J, Smith R, & Schooler JW (2009). Experience sampling during fMRI reveals default network and executive system contributions to mind wandering. Proceedings of the National Academy of Sciences, U.S.A, 106, 8719–8724.
    1. Cocchi L, Sale MV, Lord A, Zalesky A, Breakspear M, & Mattingley JB (2015). Dissociable effects of local inhibitory and excitatory theta-burst stimulation on large-scale brain dynamics. Journal of Neurophysiology, 113, 3375–3385.
    1. Davachi L (2006). Item, context and relational episodic encoding in humans. Current Opinion in Neurobiology, 16, 693–700.
    1. Diana RA, Yonelinas AP, & Ranganath C (2007). Imaging recollection and familiarity in the medial temporal lobe: A three-component model. Trends in Cognitive Sciences, 11, 379–386.
    1. Ding S-L, Van Hoesen GW, & Rockland KS (2000). Inferior parietal lobule projections to the presubiculum and neighboring ventromedial temporal cortical areas. Journal of Comparative Neurology, 425, 510–530.
    1. Eichenbaum H, Yonelinas AP, & Ranganath C (2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30, 123–152.
    1. Eldaief MC, Halko MA, Buckner RL, & Pascual-Leone A (2011). Transcranial magnetic stimulation modulates the brain’s intrinsic activity in a frequency-dependent manner. Proceedings of the National Academy of Sciences, U.S.A, 108, 21229–21234.
    1. Esterman M, Thai M, Okabe H, DeGutis J, Saad E, Laganiere SE, et al. (2017). Network-targeted cerebellar transcranial magnetic stimulation improves attentional control. Neuroimage, 156, 190–198.
    1. Fox MD, Halko MA, Eldaief MC, & Pascual-Leone A (2012). Measuring and manipulating brain connectivity with resting state functional connectivity magnetic resonance imaging (fcMRI) and transcranial magnetic stimulation (TMS). Neuroimage, 62, 2232–2243.
    1. Fox MD, Snyder AZ, Vincent JL, Corbetta M, Van Essen DC, & Raichle ME (2005). The human brain is intrinsically organized into dynamic, anticorrelated functional networks. Proceedings of the National Academy of Sciences, U.S.A, 102, 9673–9678.
    1. Gorgolewski KJ, Varoquaux G, Rivera G, Schwarz Y, Ghosh SS, Maumet C, et al. (2015). : A web-based repository for collecting and sharing unthresholded statistical maps of the human brain. Frontiers in Neuroinformatics, 9, 8.
    1. Gratton C, Lee TG, Nomura EM, & D’Esposito M (2013). The effect of theta-burst TMS on cognitive control networks measured with resting state fMRI. Frontiers in Systems Neuroscience, 7, 124.
    1. Gratton C, Lee TG, Nomura EM, & D’Esposito M (2014). Perfusion MRI indexes variability in the functional brain effects of theta-burst transcranial magnetic stimulation. PLoS One, 9, e101430.
    1. Hales JB, & Brewer JB (2013). Parietal and frontal contributions to episodic encoding of location. Behavioural Brain Research, 243, 16–20.
    1. Halko MA, Farzan F, Eldaief MC, Schmahmann JD, & Pascual-Leone A (2014). Intermittent theta-burst stimulation of the lateral cerebellum increases functional connectivity of the default network. Journal of Neuroscience, 34, 12049–12056.
    1. Hannula DE, & Ranganath C (2008). Medial temporal lobe activity predicts successful relational memory binding. Journal of Neuroscience, 28, 116–124.
    1. Harlow IM, & Yonelinas AP (2016). Distinguishing between the success and precision of recollection. Memory, 24, 114–127.
    1. Hayes SM, Salat DH, & Verfaellie M (2012). Default network connectivity in medial temporal lobe amnesia. Journal of Neuroscience, 32, 14622–14629.
    1. Holdstock JS, Mayes AR, Gong QY, Roberts N, & Kapur N (2005). Item recognition is less impaired than recall and associative recognition in a patient with selective hippocampal damage. Hippocampus, 15, 203–215.
    1. Hoogendam JM, Ramakers GMJ, & Di Lazzaro V (2010). Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimulation, 3, 95–118.
    1. Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, & Rothwell JC (2005). Theta burst stimulation of the human motor cortex. Neuron, 45, 201–206.
    1. Hubl D, Nyffeler T, Wurtz P, Chaves S, Pflugshaupt T, Lüthi M, et al. (2008). Time course of blood oxygenation level-dependent signal response after theta burst transcranial magnetic stimulation of the frontal eye field. Neuroscience, 151, 921–928.
    1. Husain M, & Nachev P (2007). Space and the parietal cortex. Trends in Cognitive Sciences, 11, 30–36.
    1. Hutchinson JB, Uncapher MR, & Wagner AD (2009). Posterior parietal cortex and episodic retrieval: Convergent and divergent effects of attention and memory. Learning & Memory, 16, 343–356.
    1. Jannati A, Block G, Oberman LM, Rotenberg A, & Pascual-Leone A (2017). Interindividual variability in response to continuous theta-burst stimulation (cTBS) in healthy adults. Clinical Neurophysiology, 128, 2268–2278.
    1. Kahn I, Andrews-Hanna JR, Vincent JL, Snyder AZ, & Buckner RL (2008). Distinct cortical anatomy linked to subregions of the medial temporal lobe revealed by intrinsic functional connectivity. Journal of Neurophysiology, 100, 129–139.
    1. Kim H (2011). Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies. Neuroimage, 54, 2446–2461.
    1. Kim H (2013). Differential neural activity in the recognition of old versus new events: An activation likelihood estimation meta-analysis. Human Brain Mapping, 34, 814–836.
    1. Kobayashi Y, & Amaral DG (2003). Macaque monkey retrosplenial cortex: II. Cortical afferents. Journal of Comparative Neurology, 466, 48–79.
    1. Kobayashi Y, & Amaral DG (2007). Macaque monkey retrosplenial cortex: III. Cortical efferents. Journal of Comparative Neurology, 502, 810–833.
    1. Koen JD, & Yonelinas AP (2016). Recollection, not familiarity, decreases in healthy aging: Converging evidence from four estimation methods. Memory, 24, 75–88.
    1. LaJoie R, Landeau B, Perrotin A, Bejanin A, Egret S, Pélerin A, et al. (2014). Intrinsic connectivity identifies the hippocampus as a main crossroad between Alzheimer’s and semantic dementia-targeted networks. Neuron, 81, 1417–1428.
    1. Lee H, Chun MM, & Kuhl BA (2017). Lower parietal encoding activation is associated with sharper information and better memory. Cerebral Cortex, 27, 2486–2499.
    1. Lee TG, & D’Esposito M (2012). The dynamic nature of top–down signals originating from prefrontal cortex: A combined fMRI-TMS study. Journal of Neuroscience, 32, 15458–15466.
    1. Maguire EA, & Mullally SL (2013). The hippocampus: A manifesto for change. Journal of Experimental Psychology: General, 142, 1180–1189.
    1. Mason MF, Norton MI, Van Horn JD, Wegner DM, Grafton ST, & Macrae CN (2007). Wandering minds: The default network and stimulus-independent thought. Science, 315, 393–395.
    1. Mayes A, Montaldi D, & Migo E (2007). Associative memory and the medial temporal lobes. Trends in Cognitive Sciences, 11, 126–135.
    1. Muschelli J, Nebel MB, Caffo BS, Barber AD, Pekar JJ, & Mostofsky SH (2014). Reduction of motion-related artifacts in resting state fMRI using aCompCor. Neuroimage, 96, 22–35.
    1. Nee DE, & D’Esposito M (2017). Causal evidence for lateral prefrontal cortex dynamics supporting cognitive control. eLife, 6, e28040.
    1. Nilakantan AS, Bridge DJ, Gagnon EP, VanHaerents SA, & Voss JL (2017). Stimulation of the posterior cortical–hippocampal network enhances precision of memory recollection. Current Biology, 27, 465–470.
    1. Nunn JA, Graydon FJX, Polkey CE, & Morris RGM (1999). Differential spatial memory impairment after right temporal lobectomy demonstrated using temporal titration. Brain, 122, 47–59.
    1. Oberman L, Edwards D, Eldaief M, & Pascual-Leone A (2011). Safety of theta burst transcranial magnetic stimulation: A systematic review of the literature. Journal of Clinical Neurophysiology, 28, 67–74.
    1. Olsen RK, Moses SN, Riggs L, & Ryan JD (2012). The hippocampus supports multiple cognitive processes through relational binding and comparison. Frontiers in Human Neuroscience, 6, 146.
    1. Piekema C, Kessels RPC, Mars RB, Petersson KM, & Fernández G (2006). The right hippocampus participates in short-term memory maintenance of object–location associations. Neuroimage, 33, 374–382.
    1. Power JD, Plitt M, Laumann TO, & Martin A (2017). Sources and implications of whole-brain fMRI signals in humans. Neuroimage, 146, 609–625.
    1. Pruessner JC, Li LM, Serles W, Pruessner M, Collins DL, Kabani N, et al. (2000). Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: Minimizing the discrepancies between laboratories. Cerebral Cortex, 10, 433–442.
    1. Rahnev D, Nee DE, Riddle J, Larson AS, & D’Esposito M (2016). Causal evidence for frontal cortex organization for perceptual decision making. Proceedings of the National Academy of Sciences, U.S.A, 113, 6059–6064.
    1. Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, & Shulman GL (2001). A default mode of brain function. Proceedings of the National Academy of Sciences, U.S.A, 98, 676–682.
    1. Ranganath C, & Ritchey M (2012). Two cortical systems for memory-guided behaviour. Nature Reviews Neuroscience, 13, 713–726.
    1. Ranganath C, Yonelinas AP, Cohen MX, Dy CJ, Tom SM, & D’Esposito M (2004). Dissociable correlates of recollection and familiarity within the medial temporal lobes. Neuropsychologia, 42, 2–13.
    1. Richter FR, Cooper RA, Bays PM, & Simons JS (2016). Distinct neural mechanisms underlie the success, precision, and vividness of episodic memory. eLife, 5, e18260.
    1. Ritchey M, Yonelinas AP, & Ranganath C (2014). Functional connectivity relationships predict similarities in task activation and pattern information during associative memory encoding. Journal of Cognitive Neuroscience, 26, 1085–1099.
    1. Rockland KS, & Van Hoesen GW (1999). Some temporal and parietal cortical connections converge in CA1 of the primate hippocampus. Cerebral Cortex, 9, 232–237.
    1. Romei V, Bauer M, Brooks JL, Economides M, Penny W, Thut G, et al. (2016). Causal evidence that intrinsic beta-frequency is relevant for enhanced signal propagation in the motor system as shown through rhythmic TMS. Neuroimage, 126, 120–130.
    1. Ruff CC, Driver J, & Bestmann S (2009). Combining TMS and fMRI: From “virtual lesions” to functional-network accounts of cognition. Cortex, 45, 1043–1049.
    1. Rugg MD, & King DR (2017). Ventral lateral parietal cortex and episodic memory retrieval. Cortex, 1–13.
    1. Schaefer A, Kong R, Gordon EM, Laumann TO, Zuo X-N, Holmes AJ, et al. (2017). Local–global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI. Cerebral Cortex.
    1. Schneegans S, & Bays PM (2016). No fixed item limit in visuospatial working memory. Cortex, 83, 181–193.
    1. Scoville WB, & Milner B (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry, 20, 11–21.
    1. Seghier ML (2013). The angular gyrus: Multiple functions and multiple subdivisions. The Neuroscientist, 19, 43–61.
    1. Selemon LD, & Goldman-Rakic PS (1988). Common cortical and subcortical targets of the dorsolateral prefrontal and posterior parietal cortices in the rhesus monkey: Evidence for a distributed neural network subserving spatially guided behavior. Journal of Neuroscience, 8, 4049–4068.
    1. Seltzer B, & Pandya DN (1984). Further observations on parieto-temporal connections in the rhesus monkey. Experimental Brain Research, 55, 301–312.
    1. Seltzer B, & Van Hoesen GW (1979). A direct inferior parietal lobule projection to the presubiculum in the rhesus monkey. Brain Research, 179, 157–161.
    1. Sestieri C, Capotosto P, Tosoni A, Romani GL, & Corbetta M (2013). Interference with episodic memory retrieval following transcranial stimulation of the inferior but not the superior parietal lobule. Neuropsychologia, 51, 900–906.
    1. Sestieri C, Corbetta M, Romani GL, & Shulman GL (2011). Episodic memory retrieval, parietal cortex, and the default mode network: Functional and topographic analyses. Journal of Neuroscience, 31, 4407–4420.
    1. Sestieri C, Shulman GL, & Corbetta M (2010). Attention to memory and the environment: Functional specialization and dynamic competition in human posterior parietal cortex. Journal of Neuroscience, 30, 8445–8456.
    1. Sestieri C, Shulman GL, & Corbetta M (2017). The contribution of the human posterior parietal cortex to episodic memory. Nature Reviews Neuroscience, 18, 183–192.
    1. Smallwood J, Baracaia SF, Lowe M, & Obonsawin M (2003). Task unrelated thought whilst encoding information. Consciousness and Cognition, 12, 452–484.
    1. Smith ML, & Milner B (1981). The role of the right hippocampus in the recall of spatial location. Neuropsychologia, 19, 781–793.
    1. Smith ML, & Milner B (1989). Right hippocampal impairment in the recall of spatial location: Encoding deficit or rapid forgetting? Neuropsychologia, 27, 71–81.
    1. Sommer T, Rose M, Gläscher J, Wolbers T, & Büchel C (2005). Dissociable contributions within the medial temporal lobe to encoding of object-location associations. Learning & Memory, 12, 343–351.
    1. Sommer T, Rose M, Weiller C, & Büchel C (2005). Contributions of occipital, parietal and parahippocampal cortex to encoding of object–location associations. Neuropsychologia, 43, 732–743.
    1. Squire LR (1992). Memory and the hippocampus: A synthesis from findings with rats, monkeys, and humans. Psychological Review, 99, 195–231.
    1. Stagg CJ, Wylezinska M, Matthews PM, Johansen-Berg H, Jezzard P, Rothwell JC, et al. (2009). Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. Journal of Neurophysiology, 101, 2872–2877.
    1. Staresina BP, Cooper E, & Henson RN (2013). Reversible information flow across the medial temporal lobe: The hippocampus links cortical modules during memory retrieval. Journal of Neuroscience, 33, 14184–14192.
    1. Stepankova K, Fenton AA, Pastalkova E, Kalina M, & Bohbot VD (2004). Object–location memory impairment in patients with thermal lesions to the right or left hippocampus. Neuropsychologia, 42, 1017–1028.
    1. Strafella AP, Paus T, Barrett J, & Dagher A (2001). Repetitive transcranial magnetic stimulation of the human prefrontal cortex induces dopamine release in the caudate nucleus. Journal of Neuroscience, 21, RC157.
    1. Strafella AP, Paus T, Fraraccio M, & Dagher A (2003). Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain, 126, 2609–2615.
    1. Sun SZ, Fidalgo C, Barense MD, Lee ACH, Cant JS, & Ferber S (2017). Erasing and blurring memories: The differential impact of interference on separate aspects of forgetting. Journal of Experimental Psychology: General, 146, 1606–1630.
    1. Suppa A, Huang Y-Z, Funke K, Ridding MC, Cheeran B, Di Lazzaro V, et al. (2016). Ten years of theta burst stimulation in humans: Established knowledge, unknowns and prospects. Brain Stimulation, 9, 323–335.
    1. Suppa A, Ortu E, Zafar N, Deriu F, Paulus W, Berardelli A, et al. (2008). Theta burst stimulation induces after-effects on contralateral primary motor cortex excitability in humans. Journal of Physiology, 586, 4489–4500.
    1. Suzuki WA, & Amaral DG (1994). Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents. Journal of Comparative Neurology, 350, 497–533.
    1. Tambini A, & Davachi L (2013). Persistence of hippocampal multivoxel patterns into postencoding rest is related to memory. Proceedings of the National Academy of Sciences, U.S.A, 110, 19591–19596.
    1. Thakral PP, Madore KP, & Schacter DL (2017). A role for the left angular gyrus in episodic simulation and memory. Journal of Neuroscience, 37, 8142–8149.
    1. Uddin LQ, Supekar K, Amin H, Rykhlevskaia E, Nguyen DA, Greicius MD, et al. (2010). Dissociable connectivity within human angular gyrus and intraparietal sulcus: Evidence from functional and structural connectivity. Cerebral Cortex, 20, 2636–2646.
    1. Uncapher MR, & Wagner AD (2009). Posterior parietal cortex and episodic encoding: Insights from fMRI subsequent memory effects and dual-attention theory. Neurobiology of Learning and Memory, 91, 139–154.
    1. Valchev N, Ćurčić-Blake B, Renken RJ, Avenanti A, Keysers C, Gazzola V, et al. (2015). cTBS delivered to the left somatosensory cortex changes its functional connectivity during rest. Neuroimage, 114, 386–397.
    1. van Asselen M, Kessels RPC, Frijns CJM, Kappelle LJ, Neggers SFW, & Postma A (2009). Object-location memory: A lesion–behavior mapping study in stroke patients. Brain and Cognition, 71, 287–294.
    1. Vann SD, Aggleton JP, & Maguire EA (2009). What does the retrosplenial cortex do? Nature Reviews Neuroscience, 10, 792–802.
    1. Vercammen A, Knegtering H, Liemburg EJ, den Boer JA, & Aleman A (2010). Functional connectivity of the temporo-parietal region in schizophrenia: Effects of rTMS treatment of auditory hallucinations. Journal of Psychiatric Research, 44, 725–731.
    1. Vilberg KL, & Rugg MD (2008). Memory retrieval and the parietal cortex: A review of evidence from a dual-process perspective. Neuropsychologia, 46, 1787–1799.
    1. Vincent JL, Snyder AZ, Fox MD, Shannon BJ, Andrews JR, Raichle ME, et al. (2006). Coherent spontaneous activity identifies a hippocampal–parietal memory network. Journal of Neurophysiology, 96, 3517–3531.
    1. Wagner AD, Shannon BJ, Kahn I, & Buckner RL (2005). Parietal lobe contributions to episodic memory retrieval. Trends in Cognitive Sciences, 9, 445–453.
    1. Wang JX, Rogers LM, Gross EZ, Ryals AJ, Dokucu ME, Brandstatt KL, et al. (2014). Targeted enhancement of cortical–hippocampal brain networks and associative memory. Science, 345, 1054–1057.
    1. Wang JX, & Voss JL (2015). Long-lasting enhancements of memory and hippocampal–cortical functional connectivity following multiple-day targeted noninvasive stimulation. Hippocampus, 25, 877–883.
    1. Wang S-F, Ritchey M, Libby L, & Ranganath C (2016). Functional connectivity based parcellation of the human medial temporal lobe. Neurobiology of Learning and Memory, 134, 123–134.
    1. Watanabe T, Hanajima R, Shirota Y, Ohminami S, Tsutsumi R, Terao Y, et al. (2014). Bidirectional effects on interhemispheric resting-state functional connectivity induced by excitatory and inhibitory repetitive transcranial magnetic stimulation. Human Brain Mapping, 35, 1896–1905.
    1. Wischnewski M, & Schutter DJLG (2015). Efficacy and time course of theta burst stimulation in healthy humans. Brain Stimulation, 8, 685–692.
    1. Yazar Y, Bergström ZM, & Simons JS (2014). Continuous theta burst stimulation of angular gyrus reduces subjective recollection. PLoS One, 9, e110414.
    1. Yazar Y, Bergström ZM, & Simons JS (2017). Reduced multimodal integration of memory features following continuous theta burst stimulation of angular gyrus. Brain Stimulation, 10, 624–629.
    1. Yeo BTT, Krienen FM, Chee MWL, & Buckner RL (2014). Estimates of segregation and overlap of functional connectivity networks in the human cerebral cortex. Neuroimage, 88, 212–227.
    1. Yeo BTT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M, et al. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106, 1125–1165.
    1. Yonelinas AP (2013). The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory. Behavioural Brain Research, 254, 34–44.
    1. Yonelinas AP, & Jacoby LL (1995). The relation between remembering and knowing as bases for recognition: Effects of size congruency. Journal of Memory and Language, 34, 622–643.
    1. Zimmermann K, & Eschen A (2017). Brain regions involved in subprocesses of small-space episodic object-location memory: A systematic review of lesion and functional neuroimaging studies. Memory, 25, 487–519.

Source: PubMed

Sponsoren und Mitarbeiter

Krankheiten

Drogeninterventionen

3
Abonnieren