Neural Dynamics of Visual Stream Interactions During Memory-Guided Actions Investigated by Intracranial EEG
Status Publisher Jazyk angličtina Země Singapur Médium print-electronic
Typ dokumentu časopisecké články
PubMed
40095210
DOI
10.1007/s12264-025-01371-x
PII: 10.1007/s12264-025-01371-x
Knihovny.cz E-zdroje
- Klíčová slova
- Alpha oscillations, Dorsal visual stream, Granger causality analysis, Intracranial EEG, Memory-guided actions, Phase-locking value, Theta oscillations, Ventral visual stream,
- Publikační typ
- časopisecké články MeSH
The dorsal and ventral visual streams have been considered to play distinct roles in visual processing for action: the dorsal stream is assumed to support real-time actions, while the ventral stream facilitates memory-guided actions. However, recent evidence suggests a more integrated function of these streams. We investigated the neural dynamics and functional connectivity between them during memory-guided actions using intracranial EEG. We tracked neural activity in the inferior parietal lobule in the dorsal stream, and the ventral temporal cortex in the ventral stream as well as the hippocampus during a delayed action task involving object identity and location memory. We found increased alpha power in both streams during the delay, indicating their role in maintaining spatial visual information. In addition, we recorded increased alpha power in the hippocampus during the delay, but only when both object identity and location needed to be remembered. We also recorded an increase in theta band phase synchronization between the inferior parietal lobule and ventral temporal cortex and between the inferior parietal lobule and hippocampus during the encoding and delay. Granger causality analysis indicated dynamic and frequency-specific directional interactions among the inferior parietal lobule, ventral temporal cortex, and hippocampus that varied across task phases. Our study provides unique electrophysiological evidence for close interactions between dorsal and ventral streams, supporting an integrated processing model in which both streams contribute to memory-guided actions.
3rd Faculty of Medicine Charles University Prague Czechia
Klinik für Neurochirurgie Universitätsspital Zürich Universität Zürich Zurich Switzerland
Zobrazit více v PubMed
Goodale MA, Milner AD. Separate visual pathways for perception and action. Trends Neurosci 1992, 15: 20–25. PubMed DOI
Goodale MA, Westwood DA, David Milner A. Two distinct modes of control for object-directed action. Prog Brain Res 2004, 144: 131–144. PubMed DOI
Milner AD, Goodale MA. Two visual systems re-viewed. Neuropsychologia 2008, 46: 774–785. PubMed DOI
Baddeley A. Working memory: Looking back and looking forward. Nat Rev Neurosci 2003, 4: 829–839. PubMed DOI
Milner AD, Paulignan Y, Dijkerman HC, Michel F, Jeannerod M. A paradoxical improvement of misreaching in optic Ataxia: New evidence for two separate neural systems for visual localization. Proc Biol Sci 1999, 266: 2225–2229. PubMed DOI PMC
Singhal A, Monaco S, Kaufman LD, Culham JC. Human fMRI reveals that delayed action re-recruits visual perception. PLoS One 2013, 8: e73629. PubMed DOI PMC
Cohen NR, Cross ES, Tunik E, Grafton ST, Culham JC. Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: A TMS approach. Neuropsychologia 2009, 47: 1553–1562. PubMed DOI
Hsieh LT, Ekstrom AD, Ranganath C. Neural oscillations associated with item and temporal order maintenance in working memory. J Neurosci 2011, 31: 10803–10810. PubMed DOI PMC
Johnson EL, King-Stephens D, Weber PB, Laxer KD, Lin JJ, Knight RT. Spectral imprints of working memory for everyday associations in the frontoparietal network. Front Syst Neurosci 2019, 12: 65. PubMed DOI PMC
Lee B, Kim JS, Chung CK. Parietal and medial temporal lobe interactions in working memory goal-directed behavior. Cortex 2022, 150: 126–136. PubMed DOI
Himmelbach M, Nau M, Zündorf I, Erb M, Perenin MT, Karnath HO. Brain activation during immediate and delayed reaching in optic Ataxia. Neuropsychologia 2009, 47: 1508–1517. PubMed DOI
Fiehler K, Bannert MM, Bischoff M, Blecker C, Stark R, Vaitl D. Working memory maintenance of grasp-target information in the human posterior parietal cortex. Neuroimage 2011, 54: 2401–2411. PubMed DOI
Schenk T, Hesse C. Do we have distinct systems for immediate and delayed actions? A selective review on the role of visual memory in action. Cortex 2018, 98: 228–248. PubMed DOI
Yonelinas AP. The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory. Behav Brain Res 2013, 254: 34–44. PubMed DOI PMC
Ekstrom AD, Yonelinas AP. Precision, binding, and the hippocampus: Precisely what are we talking about? Neuropsychologia 2020, 138: 107341. PubMed DOI PMC
Borders AA, Ranganath C, Yonelinas AP. The hippocampus supports high-precision binding in visual working memory. Hippocampus 2022, 32: 217–230. PubMed DOI
Boran E, Fedele T, Klaver P, Hilfiker P, Stieglitz L, Grunwald T, et al. Persistent hippocampal neural firing and hippocampal-cortical coupling predict verbal working memory load. Sci Adv 2019, 5: eaav3687. PubMed DOI PMC
Su M, Hu K, Liu W, Wu Y, Wang T, Cao C, et al. Theta oscillations support prefrontal-hippocampal interactions in sequential working memory. Neurosci Bull 2024, 40: 147–156. PubMed DOI
Fries P. Rhythms for cognition: Communication through coherence. Neuron 2015, 88: 220–235. PubMed DOI PMC
Pesaran B, Vinck M, Einevoll GT, Sirota A, Fries P, Siegel M, et al. Investigating large-scale brain dynamics using field potential recordings: Analysis and interpretation. Nat Neurosci 2018, 21: 903–919. PubMed DOI PMC
Sarnthein J, Petsche H, Rappelsberger P, Shaw GL, von Stein A. Synchronization between prefrontal and posterior association cortex during human working memory. Proc Natl Acad Sci U S A 1998, 95: 7092–7096. PubMed DOI PMC
Solomon EA, Kragel JE, Sperling MR, Sharan A, Worrell G, Kucewicz M, et al. Widespread Theta synchrony and high-frequency desynchronization underlies enhanced cognition. Nat Commun 2017, 8: 1704. PubMed DOI PMC
Bastos AM, Schoffelen JM. A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front Syst Neurosci 2016, 9: 175. PubMed DOI PMC
Dimakopoulos V, Mégevand P, Stieglitz LH, Imbach L, Sarnthein J. Information flows from hippocampus to auditory cortex during replay of verbal working memory items. Elife 2022, 11: e78677. PubMed DOI PMC
Moraresku S, Vlcek K. The use of egocentric and allocentric reference frames in static and dynamic conditions in humans. Physiol Res 2020, 69: 787–801. PubMed DOI PMC
Dempsey LA, Cooper RJ, Roque T, Correia T, Magee E, Powell S, et al. Data-driven approach to optimum wavelength selection for diffuse optical imaging. J Biomed Opt 2015, 20: 016003. PubMed DOI
Peirce J, Gray JR, Simpson S, MacAskill M, Höchenberger R, Sogo H, et al. PsychoPy2: Experiments in behavior made easy. Behav Res Methods 2019, 51: 195–203. PubMed DOI PMC
Janca R, Tomasek M, Kalina A, Marusic P, Krsek P, Lesko R. Automated identification of stereoelectroencephalography contacts and measurement of factors influencing accuracy of frame stereotaxy. IEEE J Biomed Health Inform 2023, 27: 3326–3336. PubMed DOI
Trongnetrpunya A, Nandi B, Kang D, Kocsis B, Schroeder CE, Ding M. Assessing granger causality in electrophysiological data: Removing the adverse effects of common signals via bipolar derivations. Front Syst Neurosci 2016, 9: 189. PubMed DOI PMC
Vlcek K, Fajnerova I, Nekovarova T, Hejtmanek L, Janca R, Jezdik P, et al. Mapping the scene and object processing networks by intracranial EEG. Front Hum Neurosci 2020, 14: 561399. PubMed DOI PMC
Moraresku S, Hammer J, Janca R, Jezdik P, Kalina A, Marusic P, et al. Timing of allocentric and egocentric spatial processing in human intracranial EEG. Brain Topogr 2023, 36: 870–889. PubMed DOI PMC
Gunia A, Moraresku S, Janča R, Ježdík P, Kalina A, Hammer J, et al. The brain dynamics of visuospatial perspective-taking captured by intracranial EEG. Neuroimage 2024, 285: 120487. PubMed DOI
Miller KJ, Honey CJ, Hermes D, Rao RPN, DenNijs M, Ojemann JG. Broadband changes in the cortical surface potential track activation of functionally diverse neuronal populations. Neuroimage 2014, 85(Pt 2): 711–720. PubMed DOI
Janca R, Jezdik P, Cmejla R, Tomasek M, Worrell GA, Stead M, et al. Detection of interictal epileptiform discharges using signal envelope distribution modelling: Application to epileptic and non-epileptic intracranial recordings. Brain Topogr 2015, 28: 172–183. PubMed DOI
Lachaux JP, Rodriguez E, Martinerie J, Varela FJ. Measuring phase synchrony in brain signals. Hum Brain Mapp 1999, 8: 194–208. PubMed DOI PMC
Oostenveld R, Fries P, Maris E, Schoffelen JM. FieldTrip: Open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011, 2011: 156869. PubMed DOI
Park YM, Park J, Baek JH, Kim SI, Kim IY, Kang JK, et al. Differences in Theta coherence between spatial and nonspatial attention using intracranial electroencephalographic signals in humans. Hum Brain Mapp 2019, 40: 2336–2346. PubMed DOI PMC
Jenison RL. Directional influence between the human amygdala and orbitofrontal cortex at the time of decision-making. PLoS One 2014, 9: e109689. PubMed DOI PMC
Galati G, Lobel E, Vallar G, Berthoz A, Pizzamiglio L, Le Bihan D. The neural basis of egocentric and allocentric coding of space in humans: A functional magnetic resonance study. Exp Brain Res 2000, 133: 156–164. PubMed DOI
Saj A, Cojan Y, Musel B, Honoré J, Borel L, Vuilleumier P. Functional neuro-anatomy of egocentric versus allocentric space representation. Neurophysiol Clin 2014, 44: 33–40. PubMed DOI
Ruotolo F, Ruggiero G, Raemaekers M, Iachini T, van der Ham IM, Fracasso A, et al. Neural correlates of egocentric and allocentric frames of reference combined with metric and non-metric spatial relations. Neuroscience 2019, 409: 235–252. PubMed DOI
Goodale MA, Haffenden A. Frames of reference for perception and action in the human visual system. Neurosci Biobehav Rev 1998, 22: 161–172. PubMed DOI
Hay L, Redon C. Response delay and spatial representation in pointing movements. Neurosci Lett 2006, 408: 194–198. PubMed DOI
Chen Y, Byrne P, Douglas Crawford J. Time course of allocentric decay, egocentric decay, and allocentric-to-egocentric conversion in memory-guided reach. Neuropsychologia 2011, 49: 49–60. PubMed DOI
Ilardi CR, Iavarone A, Villano I, Rapuano M, Ruggiero G, Iachini T, et al. Egocentric and allocentric spatial representations in a patient with Bálint-like syndrome: A single-case study. Cortex 2021, 135: 10–16. PubMed DOI
Pfurtscheller G, Stancák A Jr, Neuper C. Event-related synchronization (ERS) in the alpha band—an electrophysiological correlate of cortical idling: A review. Int J Psychophysiol 1996, 24: 39–46. PubMed DOI
Sauseng P, Klimesch W, Doppelmayr M, Pecherstorfer T, Freunberger R, Hanslmayr S. EEG alpha synchronization and functional coupling during top-down processing in a working memory task. Hum Brain Mapp 2005, 26: 148–155. PubMed DOI PMC
Klimesch W, Sauseng P, Hanslmayr S. EEG alpha oscillations: The inhibition-timing hypothesis. Brain Res Rev 2007, 53: 63–88. PubMed DOI
Klimesch W. Alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci 2012, 16: 606–617. PubMed DOI PMC
Hammer J, Kajsova M, Kalina A, Krysl D, Fabera P, Kudr M, et al. Antagonistic behavior of brain networks mediated by low-frequency oscillations: Electrophysiological dynamics during internal–external attention switching. Commun Biol 2024, 7: 1105. PubMed DOI PMC
Jensen O, Gelfand J, Kounios J, Lisman JE. Oscillations in the alpha band (9–12 Hz) increase with memory load during retention in a short-term memory task. Cereb Cortex 2002, 12: 877–882. PubMed DOI
Pacheco-Estefan D, Fellner MC, Kunz L, Zhang H, Reinacher P, Roy C, et al. Maintenance and transformation of representational formats during working memory prioritization. Nat Commun 2024, 15: 8234. PubMed DOI PMC
Sederberg PB, Kahana MJ, Howard MW, Donner EJ, Madsen JR. Theta and gamma oscillations during encoding predict subsequent recall. J Neurosci 2003, 23: 10809–10814. PubMed DOI PMC
Caplan JB, Glaholt MG. The roles of EEG oscillations in learning relational information. Neuroimage 2007, 38: 604–616. PubMed DOI
Herweg NA, Solomon EA, Kahana MJ. Theta oscillations in human memory. Trends Cogn Sci 2020, 24: 208–227. PubMed DOI PMC
Joensen BH, Bush D, Vivekananda U, Horner AJ, Bisby JA, Diehl B, et al. Hippocampal Theta activity during encoding promotes subsequent associative memory in humans. Cereb Cortex 2023, 33: 8792–8802. PubMed DOI PMC
Foxe JJ, Snyder AC. The role of alpha-band brain oscillations as a sensory suppression mechanism during selective attention. Front Psychol 2011, 2: 154. PubMed DOI PMC
Babiloni C, Del Percio C, Arendt-Nielsen L, Soricelli A, Romani GL, Rossini PM, et al. Cortical EEG alpha rhythms reflect task-specific somatosensory and motor interactions in humans. Clin Neurophysiol 2014, 125: 1936–1945. PubMed DOI
Magosso E, De Crescenzio F, Ricci G, Piastra S, Ursino M. EEG alpha power is modulated by attentional changes during cognitive tasks and virtual reality immersion. Comput Intell Neurosci 2019, 2019: 7051079. PubMed DOI PMC
Cichy RM, Chen Y, Haynes JD. Encoding the identity and location of objects in human LOC. NeuroImage 2011, 54: 2297–2307. PubMed DOI
Grill-Spector K, Weiner KS. The functional architecture of the ventral temporal cortex and its role in categorization. Nat Rev Neurosci 2014, 15: 536–548. PubMed DOI PMC
Ray D, Hajare N, Roy D, Banerjee A. Large-scale functional integration, rather than functional dissociation along dorsal and ventral streams, underlies visual perception and action. J Cogn Neurosci 2020, 32: 847–861. PubMed DOI
Axmacher N, Mormann F, Fernández G, Cohen MX, Elger CE, Fell J. Sustained neural activity patterns during working memory in the human medial temporal lobe. J Neurosci 2007, 27: 7807–7816. PubMed DOI PMC
Boran E, Hilfiker P, Stieglitz L, Sarnthein J, Klaver P. Persistent neuronal firing in the medial temporal lobe supports performance and workload of visual working memory in humans. Neuroimage 2022, 254: 119123. PubMed DOI
Olson IR, Page K, Moore KS, Chatterjee A, Verfaellie M. Working memory for conjunctions relies on the medial temporal lobe. J Neurosci 2006, 26: 4596–4601. PubMed DOI PMC
Lega BC, Jacobs J, Kahana M. Human hippocampal Theta oscillations and the formation of episodic memories. Hippocampus 2012, 22: 748–761. PubMed DOI
Lisman JE, Jensen O. The Theta-gamma neural code. Neuron 2013, 77: 1002–1016. PubMed DOI PMC
Watrous AJ, Lee DJ, Izadi A, Gurkoff GG, Shahlaie K, Ekstrom AD. A comparative study of human and rat hippocampal low-frequency oscillations during spatial navigation. Hippocampus 2013, 23: 656–661. PubMed DOI PMC
Hammer J, Schirrmeister RT, Hartmann K, Marusic P, Schulze-Bonhage A, Ball T. Interpretable functional specialization emerges in deep convolutional networks trained on brain signals. J Neural Eng 2022, 19.
Lachaux JP, Rudrauf D, Kahane P. Intracranial EEG and human brain mapping. J Physiol Paris 2003, 97: 613–628. PubMed DOI