Skip to main content
SpringerLink
Log in

Functional connectivity between frontal/parietal regions and MTL–basal ganglia during feedback learning and declarative memory retrieval

  • Published:
Journal of Biosciences Aims and scope Submit manuscript

Abstract

Feedback assists the memory system in preserving the learnings from ongoing activities and updating it for future retrievals. Thus, the feedback coming from an individual's performance affects the behavior and, thereby, the performance. However, little is known regarding the interactions of learning and memory associated regions. Thus, we employ a combination of functional connectivity and neurovascular approach to explore the significance of these interactions. Our study comprises thirty-five volunteers who undergo a feedback declarative memory task using simultaneous EEG-fMRI data acquisition. Functional connectivity analysis showed that medial temporal lobe (MTL) and basal ganglia possess significant connectivity but differential relationships during feedback learning and memory retrieval. Specifically, Putamen and pallidum (sub-regions of basal ganglia) are the central hubs in these mechanisms. The neurovascular analysis reveals the increased correlation of frontal-alpha and theta powers with the bold activity of MTL during memory retrievals. The results also report the role of the frontal (and parietal) alpha-beta powers in de-synchronization (and synchronization) of the bold activity of caudate; and parietal-theta (frontal-higher-alpha) power in de-synchronization (and synchronization) of bold activity of right accumbens. Hence, the study demonstrates the significant role of the frontal-parietal EEG powers in MTL–basal ganglia relationships and neuronal adaptations during declarative memory retrieval.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  • Agrawal S, Chinnadurai V, Kaur A, Kumar P, Kaur P, Sharma R and Kumar Singh A 2019 Estimation of functional connectivity modulations during task engagement and their neurovascular underpinnings through hemodynamic reorganization method. Brain Connect. 9 341–355

    Article  PubMed  Google Scholar 

  • Allen PJ, Josephs O and Turner R 2000 A method for removing imaging artifact from continuous EEG recorded during functional MRI. NeuroImage 12 230–239

    Article  CAS  PubMed  Google Scholar 

  • Ally BA, Simons JS, McKeever JD, Peers PV and Budson AE 2008 Parietal contributions to recollection: Electrophysiological evidence from aging and patients with parietal lesions. Neuropsychologia 46 1800–1812

    Article  PubMed  PubMed Central  Google Scholar 

  • Anderson JR, Byrne D, Fincham JM and Gunn P 2008 Role of prefrontal and parietal cortices in associative learning. Cereb. Cortex 18 904–914

    Article  PubMed  Google Scholar 

  • Ashby FG, Turner BO and Horvitz JC 2010 Cortical and basal ganglia contributions to habit learning and automaticity. Trends Cogn. Sci. 14 208–215

    Article  PubMed  PubMed Central  Google Scholar 

  • Brincat SL and Miller EK 2015 Frequency-specific hippocampal-prefrontal interactions during associative learning. Nat. Neurosci. 18 576–581

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabeza R 2008 Role of parietal regions in episodic memory retrieval: The dual attentional processes hypothesis. Neuropsychologia 46 1813–1827

    Article  PubMed  PubMed Central  Google Scholar 

  • Camara E, Rodriguez-Fornells A, Ye Z and Münte TF 2009 Reward networks in the brain as captured by connectivity measures. Front. Neurosci. 3 350–362

    Article  PubMed  PubMed Central  Google Scholar 

  • Cavanagh JF and Frank MJ 2014 Frontal theta as a mechanism for cognitive control. Trends Cogn. Sci. 18 414–421

    Article  PubMed  PubMed Central  Google Scholar 

  • Chang LJ, Yarkoni T, Khaw MW and Sanfey AG 2013 Decoding the role of the insula in human cognition: Functional parcellation and large-scale reverse inference. Cereb. Cortex 23 739–749

    Article  PubMed  Google Scholar 

  • Christov II 2004 Real time electrocardiogram QRS detection using combined adaptive threshold. Biomed. Eng. Online 3 1–9

    Article  Google Scholar 

  • Cohen MX, Elger CE and Ranganath C 2007 Reward expectation modulates feedback-related negativity and EEG spectra. NeuroImage 35 968–978

    Article  PubMed  Google Scholar 

  • Cohen MX, Elger CE and Weber B 2008 Amygdala tractography predicts functional connectivity and learning during feedback-guided decision-making. NeuroImage 39 1396–1407

    Article  PubMed  Google Scholar 

  • Cohen MX, Wilmes K and van de Vijver I 2011 Cortical electrophysiological network dynamics of feedback learning. Trends Cogn. Sci. 15 558–566

    Article  PubMed  Google Scholar 

  • Cohen NJ, Poldrack RA and Eichenbaum H 1997 Memory for items and memory for relations in the procedural/declarative memory framework. Memory 5 131–178

    Article  CAS  PubMed  Google Scholar 

  • Cohn M, Moscovitch M and Davidson PSR 2010 Double dissociation between familiarity and recollection in Parkinson’s disease as a function of encoding tasks. Neuropsychologia 48 4142–4147

    Article  PubMed  Google Scholar 

  • Da Cunha C, Gomez AA and Blaha CD 2012 The role of the basal ganglia in motivated behaviour. Rev. Neurosci. 23 747–767

    Article  PubMed  CAS  Google Scholar 

  • Davachi L 2006 Item, context and relational episodic encoding in humans. Curr. Opin. Neurobiol. 16 693–700

    Article  CAS  PubMed  Google Scholar 

  • de Vanssay-Maigne A, Noulhiane M, Devauchelle AD, Rodrigo S, Baudoin-Chial S, Meder JF, Oppenheim C, Chiron C and Chassoux F 2011 Modulation of encoding and retrieval by recollection and familiarity: Mapping the medial temporal lobe networks. NeuroImage 58 1131–1138

    Article  PubMed  Google Scholar 

  • Delorme A and Makeig S 2004 EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J. Neurosci. Method. 134 9–21

    Article  Google Scholar 

  • Dobbins IG, Foley H, Schacter DL and Wagner AD 2002 Executive control during episodic retrieval. Neuron 35 989–996

    Article  CAS  PubMed  Google Scholar 

  • Doñamayor N, Marco-Pallarés J, Heldmann M, Schoenfeld MA and Münte TF 2011 Temporal dynamics of reward processing revealed by magnetoencephalography. Hum. Brain Map. 32 2228–2240

    Article  Google Scholar 

  • Eichenbaum H, Yonelinas AP and Ranganath C 2007 The medial temporal lobe and recognition memory. Annu. Rev. Neurosci. 30 123–152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Euston DR, Gruber AJ and McNaughton BL 2012 The role of medial prefrontal cortex in memory and decision making. Neuron 76 1057–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fell J, Ludowig E, Staresina BP, Wagner T, Kranz T, Elger CE and Axmacher N 2011 Medial temporal theta/alpha power enhancement precedes successful memory encoding: Evidence based on intracranial EEG. J. Neurosci. 31 5392–5397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank MJ and Claus ED 2006 Anatomy of a decision: Striato-orbitofrontal interactions in reinforcement learning, decision making and reversal. Psychol. Rev. 113 300–326

    Article  PubMed  Google Scholar 

  • Freedberg M, Toader AC, Wassermann EM and Voss JL 2020 Competitive and cooperative interactions between medial temporal and striatal learning systems. Neuropsychologia 136 107257

    Article  PubMed  Google Scholar 

  • Gabard-Durnam LJ, Leal ASM, Wilkinson CL and Levin AR 2018 The harvard automated processing pipeline for electroencephalography (HAPPE): Standardized processing software for developmental and high-artifact data. Front. Neurosci. 12 1–24

    Article  Google Scholar 

  • Gärtner M and Bajbouj M 2013 Encoding-related EEG oscillations during memory formation are modulated by mood state. Soc. Cogn. Affect. Neurosci. 9 1934–1941

    Article  Google Scholar 

  • Gerraty RT, Davidow JY, Wimmer GE, Kahn I and Shohamy D 2014 Transfer of learning relates to intrinsic connectivity between hippocampus, ventromedial prefrontal cortex and large-scale networks. J. Neurosci. 34 11297–11303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guitart-Masip M, Barnes GR, Horner A, Bauer M, Dolan RJ and Duzel E 2013 Synchronization of medial temporal lobe and prefrontal rhythms in human decision making. J. Neurosci. 33 442–451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haber SN and Knutson B 2010 The reward circuit: Linking primate anatomy and human imaging. Neuropsychopharmacology 35 4–26

    Article  PubMed  Google Scholar 

  • Han S, Huettel SA, Raposo A, Adcock RA and Dobbins IG 2010 Functional significance of striatal responses during episodic decisions: Recovery or goal attainment? J. Neurosci. 30 4767–4775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hattie J and Timperley H 2007 The power of feedback. Rev. Edu. Res. 77 81–112

    Article  Google Scholar 

  • Herweg NA, Apitz T, Leicht G, Mulert C, Fuentemilla L and Bunzeck N 2016 Theta-alpha oscillations bind the hippocampus, prefrontal cortex and striatum during recollection: Evidence from simultaneous EEG–fMRI. J. Neurosci. 36 3579–3587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hosseini AH and Holroyd CB 2015 Reward feedback stimuli elicit high-beta EEG oscillations in human dorsolateral prefrontal cortex. Sci. Rep. 5 1–8

    CAS  Google Scholar 

  • Kim KH, Yoon HW and Park HW 2004 Improved ballistocardiac artifact removal from the electroencephalogram recorded in fMRI. J. Neurosci. Method. 135 193–203

    Article  Google Scholar 

  • Knowlton BJ, Mangels JA and Squire LR 1996 A neostriatal habit learning system in humans. Science 273 1399–1402

    Article  CAS  PubMed  Google Scholar 

  • Knudsen EB and Wallis JD 2020 Closed-Loop Theta Stimulation in the Orbitofrontal Cortex Prevents Reward-Based Learning. Neuron 106 537-547.e4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee W and Reeve J 2013 Self-determined, but not non-self-determined, motivation predicts activations in the anterior insular cortex: An fMRI study of personal agency. Soc. Cogn. Affect. Neurosci. 8 538–545

    Article  PubMed  Google Scholar 

  • Luft CDB 2014 Learning from feedback: The neural mechanisms of feedback processing facilitating better performance. Behav. Brain Res. 261 356–368

    Article  PubMed  Google Scholar 

  • Maia TV 2009 Fear conditioning and social groups: Statistics, not genetics. Cog. Sci. 33 1232–1251

    Article  Google Scholar 

  • Marco-Pallares J, Cucurell D, Cunillera T, García R and andrés-Pueyo A, Münte TF and Rodríguez-Fornells A, 2008 Human oscillatory activity associated to reward processing in a gambling task. Neuropsychologia 46 241–248

    Article  PubMed  Google Scholar 

  • Miller EK and Cohen JD 2001 An integrate theory of PFC function. Annu. Rev. Neurosci. 24 167–202

    Article  CAS  PubMed  Google Scholar 

  • Moustafa AA and Gluck MA 2011 Computational cognitive models of prefrontal-striatal-hippocampal interactions in Parkinson’s disease and schizophrenia. Neural Networks 24 575–591

    Article  PubMed  Google Scholar 

  • Packard MG, White M and Ha Q 1989 Differential effects of fornix and caudate radial maze tasks: evidence for multiple nucleus lesions on two memory systems. J. Neurosci. 9 1465–1472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pasupathy A and Miller EK 2005 Different time courses of learning-related activity in the prefrontal cortex and striatum. Nature 433 873–876

    Article  CAS  PubMed  Google Scholar 

  • Peters GJ, David CN, Marcus MD and Smith DM 2013 The medial prefrontal cortex is critical for memory retrieval and resolving interference. Learn. Mem. 20 201–209

    Article  PubMed  PubMed Central  Google Scholar 

  • Poldrack RA and Rodriguez P 2004 How do memory systems interact? Evidence from human classification learning. Neurobiol. Learn. Mem. 82 324–332

    Article  PubMed  Google Scholar 

  • Preston AR and Eichenbaum H 2013a Interplay of hippocampus and prefrontal cortex in memory. Curr. Biol. 23 R764–R773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Preston AR and Eichenbaum H 2013b Interplay of hippocampus and prefrontal cortex in memory. Curr. Biol. 23 1–21

    Article  CAS  Google Scholar 

  • Pu M and Yu R 2019 Post-encoding frontal theta activity predicts incidental memory in the reward context. Neurobiol. Learn. Mem. 158 14–23

    Article  PubMed  Google Scholar 

  • Ridderinkhof KR, Van Den Wildenberg WPM, Segalowitz SJ and Carter CS 2004 Neurocognitive mechanisms of cognitive control: The role of prefrontal cortex in action selection, response inhibition, performance monitoring and reward-based learning. Brain Cogn. 56 129–140

    Article  PubMed  Google Scholar 

  • Rushworth MFS, Noonan MAP, Boorman ED, Walton ME and Behrens TE 2011 Frontal Cortex and Reward-Guided Learning and Decision-Making. Neuron 70 1054–1069

    Article  CAS  PubMed  Google Scholar 

  • Salari N and Rose M 2016 Dissociation of the functional relevance of different pre-stimulus oscillatory activity for memory formation. NeuroImage 125 1013–1021

    Article  PubMed  Google Scholar 

  • Schultz W 2000 Multiple reward signals in the brain. Nat. Rev. Neurosci. 1 199–207

    Article  CAS  PubMed  Google Scholar 

  • Schultz W 2016 Reward functions of the basal ganglia. J. Neural Transm. 123 679–693

    Article  PubMed  Google Scholar 

  • Scimeca JM and Badre D 2012 Striatal contributions to declarative memory retrieval. Neuron 75 380–392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seger CA and Cincotta CM 2006 Dynamics of frontal, striatal and hippocampal systems during rule learning. Cereb. Cortex 16 1546–1555

    Article  PubMed  Google Scholar 

  • Seger CA and Miller EK 2010 Category learning in the brain. Annu. Rev. Neurosci. 33 203–219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seger CA and Spiering BJ 2011 A critical review of habit learning and the basal ganglia. Front. Syst. Neurosci. 5 1–9

    Article  Google Scholar 

  • Shohamy D, Myers CE, Kalanithi J and Gluck MA 2008 Basal ganglia and dopamine contributions to probabilistic category learning. Neurosci. Biobehav. Rev. 32 219–236

    Article  CAS  PubMed  Google Scholar 

  • Shohamy D, Myers CE, Onlaor S and Gluck MA 2004a Role of the basal ganglia in category learning: How do patients with Parkinson’s disease learn? Behav. Neurosci. 118 676–686

    Article  CAS  PubMed  Google Scholar 

  • Shohamy Daphna and Adcock RA 2010 Dopamine and adaptive memory. Trends Cogn. Sci. 14 464–472

    Article  CAS  PubMed  Google Scholar 

  • Shohamy Daphna, Myers CE, Grossman S, Sage J, Gluck MA and Poldrack RA 2004b Cortico-striatal contributions to feedback-based learning: Converging data from neuroimaging and neuropsychology. Brain 127 851–859

    Article  CAS  PubMed  Google Scholar 

  • Simons JS and Spiers HJ 2003 Prefrontal and medial temporal lobe interactions in long-term memory. Nat. Rev. Neurosci. 4 637–648

    Article  CAS  PubMed  Google Scholar 

  • Smith KS, Tindell AJ, Aldridge JW and Berridge KC 2009 Ventral pallidum roles in reward and motivation. Behav. Brain Res. 196 155–167

    Article  PubMed  Google Scholar 

  • Squire LR, Stark CEL and Clark RE 2004 the Medial Temporal Lobe. Annu. Rev. Neurosci. 27 279–306

    Article  CAS  PubMed  Google Scholar 

  • Summerfield C and Mangels JA 2005 Functional coupling between frontal and parietal lobes during recognition memory. NeuroReport 16 117–122

    Article  PubMed  Google Scholar 

  • Tendolkar I, Arnold J, Petersson KM, Weis S, Brockhaus-Dumke A, Van Eijndhoven P, Buitelaar J and Fernández G 2008 Contributions of the medial temporal lobe to declarative memory retrieval: Manipulating the amount of contextual retrieval. Learn. Mem. 15 611–617

    Article  PubMed  Google Scholar 

  • Thibaut F 2016 Basal ganglia play a crucial role in decision making. Dialog. Clin. Neurosci. 18 3

    Article  Google Scholar 

  • Thürer B, Stockinger C, Putze F, Schultz T and Stein T 2017 Mechanisms within the parietal cortex correlate with the benefits of random practice in motor adaptation. Front. Hum. Neurosci. 11 1–11

    Article  Google Scholar 

  • Tricomi E and Fiez JA 2008 Feedback signals in the caudate reflect goal achievement on a declarative memory task. NeuroImage 41 1154–1167

    Article  PubMed  Google Scholar 

  • Tricomi E and Fiez JA 2012 Information content and reward processing in the human striatum during performance of a declarative memory task. Cogn. Affect. Behav. Neurosci. 12 361–372

    Article  PubMed  Google Scholar 

  • van de Vijver I, Richard Ridderinkhof K and Cohen MX 2011 Frontal oscillatory dynamics predict feedback learning and action adjustment. J. Cogn. Neurosci. 23 4106–4121

    Article  PubMed  Google Scholar 

  • Wagner AD, Shannon BJ, Kahn I and Buckner RL 2005 Parietal lobe contributions to episodic memory retrieval. Trends Cogn. Sci. 9 445–453

    Article  PubMed  Google Scholar 

  • Walsh ND and Phillips ML 2010 Interacting outcome retrieval, anticipation and feedback processes in the human brain. Cereb. Cortex 20 271–281

    Article  PubMed  Google Scholar 

  • Waraczynski M and Demco C 2006 Lidocaine inactivation of the ventral pallidum affects responding for brain stimulation reward more than it affects the stimulation’s reward value. Behav. Brain Res. 173 288–298

    Article  CAS  PubMed  Google Scholar 

  • Whitfield-Gabrieli S and Nieto-Castanon A 2012 Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connect. 2 125–141 Yin HH and Knowlton BJ 2006 The role of the basal ganglia in habit formation. Nature Rev. Neurosci. 7 464–476

    Google Scholar 

  • Yin HH and Knowlton BJ 2006 The role of the basal ganglia in habit formation. Nature Rev. Neurosci. 7 464–476

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. NMR Research Centre, Institute of Nuclear Medicine and Allied Sciences, Lucknow Rd, Timarpur, Delhi, 110 054, India

    Swati Agrawal & Vijayakumar Chinnadurai

  2. Delhi Technological University, Shahbad Daulatpur, Main Bawana Road, Delhi, 110 042, India

    Swati Agrawal & Rinku Sharma

Authors
  1. Swati Agrawal
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rinku Sharma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Vijayakumar Chinnadurai
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vijayakumar Chinnadurai.

Additional information

corresponding editor: Aurnab Ghose

corresponding editor: Aurnab Ghose

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PNG 7469 KB)

Supplementary file2 (DOCX 13 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Agrawal, S., Sharma, R. & Chinnadurai, V. Functional connectivity between frontal/parietal regions and MTL–basal ganglia during feedback learning and declarative memory retrieval. J Biosci 46, 75 (2021). https://doi.org/10.1007/s12038-021-00194-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12038-021-00194-y

Keywords

Search

Navigation