Hippocampal connectivity with sensorimotor cortex during volitional finger movements: Laterality and relationship to motor learning
Autoři:
Douglas D. Burman aff001
Působiště autorů:
Department of Radiology, NorthShore University HealthSystem, Evanston, Illinois, United States of America
aff001
Vyšlo v časopise:
PLoS ONE 14(9)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0222064
Souhrn
Hippocampal interactions with the motor system are often assumed to reflect the role of memory in motor learning. Here, we examine hippocampal connectivity with sensorimotor cortex during two tasks requiring paced movements, one with a mnemonic component (sequence learning) and one without (repetitive tapping). Functional magnetic resonance imaging activity was recorded from thirteen right-handed subjects; connectivity was identified from sensorimotor cortex correlations with psychophysiological interactions in hippocampal activity between motor and passive visual tasks. Finger movements in both motor tasks anticipated the timing of the metronome, reflecting cognitive control, yet evidence of motor learning was limited to the sequence learning task; nonetheless, hippocampal connectivity was observed during both tasks. Connectivity from corresponding regions in the left and right hippocampus overlapped extensively, with improved sensitivity resulting from their conjunctive (global) analysis. Positive and negative connectivity were both evident, with positive connectivity in sensorimotor cortex ipsilateral to the moving hand during unilateral movements, whereas negative connectivity was prominent in whichever hemisphere was most active during movements. Results implicate the hippocampus in volitional finger movements even in the absence of motor learning or recall.
Klíčová slova:
Biology and life sciences – Neuroscience – Cognitive science – Cognitive psychology – Learning – Cognition – Memory – Learning and memory – Psychology – Anatomy – Brain – Hippocampus – Cerebral hemispheres – Left hemisphere – Right hemisphere – Musculoskeletal system – Body limbs – Fingers – Social sciences – Medicine and health sciences – Arms – Research and analysis methods – Database and informatics methods – Bioinformatics – Sequence analysis
Zdroje
1. Bunge SA, Burrows B, Wagner AD. Prefrontal and hippocampal contributions to visual associative recognition: interactions between cognitive control and episodic retrieval. Brain & Cognition 2004;56(2):141–52.
2. Kelemen E, Fenton AA. Dynamic grouping of hippocampal neural activity during cognitive control of two spatial frames. 2010.
3. Rudner M, Ronnberg J. The role of the episodic buffer in working memory for language processing. Cognitive Processing 2008;9(1):19–28. doi: 10.1007/s10339-007-0183-x 17917753
4. Seamans JK, Floresco SB, Phillips AG. D1 receptor modulation of hippocampal-prefrontal cortical circuits integrating spatial memory with executive functions in the rat. The Journal of neuroscience 1998;18(4):1613–1621. 9454866
5. Mukamel R, Ekstrom AD, Kaplan J, Iacoboni M, Fried I. Single-neuron responses in humans during execution and observation of actions. Current biology 2010;20(8):750–756. doi: 10.1016/j.cub.2010.02.045 20381353
6. Albouy G, Sterpenich V, Balteau E, Vandewalle G, Desseilles M, Dang-Vu T, et al. Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 2008;58(2):261–272. doi: 10.1016/j.neuron.2008.02.008 18439410
7. Fernandez-Seara MA, Aznarez-Sanado M, Mengual E, Loayza FR, Pastor MA. Continuous performance of a novel motor sequence leads to highly correlated striatal and hippocampal perfusion increases. Neuroimage 2009;47(4):1797–1808. doi: 10.1016/j.neuroimage.2009.05.061 19481611
8. Gheysen F, Van Opstal F, Roggeman C, Van Waelvelde H, Fias W. Hippocampal contribution to early and later stages of implicit motor sequence learning. Experimental brain research 2010;202(4):795–807. doi: 10.1007/s00221-010-2186-6 20195849
9. Ramnani N, Toni I, Josephs O, Ashburner J, Passingham RE. Learning-and expectation-related changes in the human brain during motor learning. Journal of Neurophysiology 2000;84(6):3026–3035. doi: 10.1152/jn.2000.84.6.3026 11110829
10. Rose M, Haider H, Salari N, Buchel C. Functional dissociation of hippocampal mechanism during implicit learning based on the domain of associations. J. Neurosci. 2011;31:13739–13745. doi: 10.1523/JNEUROSCI.3020-11.2011 21957237
11. Schendan HE, Searl MM, Melrose RJ, Stern CE. An FMRI study of the role of the medial temporal lobe in implicit and explicit sequence learning. Neuron 2003;37(6):1013–1025. doi: 10.1016/s0896-6273(03)00123-5 12670429
12. Steele CJ, Penhune VB. Specific increases within global decreases: a functional magnetic resonance imaging investigation of five days of motor sequence learning. The Journal of neuroscience 2010;30(24):8332–8341. doi: 10.1523/JNEUROSCI.5569-09.2010 20554884
13. Ekstrom AD, Caplan JB, Ho E, Shattuck K, Fried I, Kahana MJ. Human hippocampal theta activity during virtual navigation. Hippocampus 2005;15(7):881–889. doi: 10.1002/hipo.20109 16114040
14. Huang Y-Z, Edwards MJ, Rounis E, Bhatia KP, Rothwell JC. Theta burst stimulation of the human motor cortex. Neuron 2005;45(2):201–206. doi: 10.1016/j.neuron.2004.12.033 15664172
15. Perfetti B, Moisello C, Landsness EC, Kvint S, Lanzafame S, Onofrj M, et al. Modulation of gamma and theta spectral amplitude and phase synchronization is associated with the development of visuo-motor learning. The Journal of Neuroscience 2011;31(41):14810–14819. doi: 10.1523/JNEUROSCI.1319-11.2011 21994398
16. Teo JTH, Swayne OBC, Cheeran B, Greenwood RJ, Rothwell JC. Human theta burst stimulation enhances subsequent motor learning and increases performance variability. Cerebral Cortex 2011;21(7):1627–1638. doi: 10.1093/cercor/bhq231 21127013
17. Wilkinson L, Teo JT, Obeso I, Rothwell JC, Jahanshahi M. The contribution of primary motor cortex is essential for probabilistic implicit sequence learning: evidence from theta burst magnetic stimulation. Journal of cognitive neuroscience 2010;22(3):427–436. doi: 10.1162/jocn.2009.21208 19301999
18. Bertram E. The relevance of kindling for human epilepsy. Epilepsia 2007;48(s2):65–74.
19. Lang CE, Schieber MH. Differential impairment of individuated finger movements in humans after damage to the motor cortex or the corticospinal tract. Journal of neurophysiology 2003;90(2):1160–1170. doi: 10.1152/jn.00130.2003 12660350
20. Lang CE, Schieber MH. Reduced muscle selectivity during individuated finger movements in humans after damage to the motor cortex or corticospinal tract. Journal of neurophysiology 2004;91(4):1722–1733. doi: 10.1152/jn.00805.2003 14668295
21. Catani M, Dell'Acqua F, Vergani F, Malik F, Hodge H, Roy P, et al. Short frontal lobe connections of the human brain. Cortex 2012;48(2):273–291. doi: 10.1016/j.cortex.2011.12.001 22209688
22. Gitelman DR, Penny WD, Ashburner J, Friston KJ. Modeling regional and psychophysiologic interactions in fMRI: the importance of hemodynamic deconvolution. Neuroimage 2003;19(1):200–207. 12781739
23. Friston KJ, Buechel C, Fink GR, Morris J, Rolls E, Dolan RJ. Psychophysiological and modulatory interactions in neuroimaging.” Neuroimage 1997;6(3): 218–229. doi: 10.1006/nimg.1997.0291 9344826
24. Hsieh L-T, Gruber MJ, Jenkins LJ, Ranganath C. Hippocampal activity patterns carry information about objects in temporal context. Neuron 2014;81(5):1165–1178. doi: 10.1016/j.neuron.2014.01.015 24607234
25. Klausberger T, Somogyi P. Neuronal Diversity and Temporal Dynamics: The Unity of Hippocampal Circuit Operations. Science 2008:53–57.
26. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H. Hippocampal "time cells" bridge the gap in memory for discontiguous events. Neuron 2011;71(4):737–749. doi: 10.1016/j.neuron.2011.07.012 21867888
27. Burman DD, Minas T, Bolger DJ, Booth JR. Age, sex, and verbal abilities affect location of linguistic connectivity in ventral visual pathway. Brain and language 2013;124(2):184–193. doi: 10.1016/j.bandl.2012.12.007 23376366
28. Li K, Guo L, Nie J, Li G, Liu T. Review of methods for functional brain connectivity detection using fMRI. Computerized Medical Imaging and Graphics 2009;2(33):131–139.
29. Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J. Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proceedings of the National Academy of Sciences 2010;107(7):3228–3233.
30. Battaglia FP, Benchenane K, Sirota A, Pennartz CMA, Wiener SI. The hippocampus: hub of brain network communication for memory. Trends in cognitive sciences 2011;15(7):310–318. doi: 10.1016/j.tics.2011.05.008 21696996
31. Jacobs J. Hippocampal theta oscillations are slower in humans than in rodents: implications for models of spatial navigation and memory. Philosophical Transactions of the Royal Society of London B: Biological Sciences 2014;369(1635):20130304. doi: 10.1098/rstb.2013.0304 24366145
32. Kaplan R, Doeller CF, Barnes GR, Litvak V, Düzel E, Bandettini PA, et al. Movement-Related Theta Rhythm in Humans: Coordinating Self-Directed Hippocampal Learning. PLoS Biology 2012;10(2).
33. Lega BC, Jacobs J, Kahana M. Human hippocampal theta oscillations and the formation of episodic memories. Hippocampus 2012;22(4):748–761. doi: 10.1002/hipo.20937 21538660
34. R_Core_Team. A language and environment for statistical computing. R Foundation for Statistical Computing 2015 2015-06-18 [cited; R version 3.2.1]:Available from: http://www.R-project.org/
35. Lee TD, Swinnen SP, Serrien DJ. Cognitive Effort and Motor Learning. 1994.
36. Hlustik P, Solodkin A, Gullapalli RP, Noll DC, Small SL. Somatotopy in human primary motor and somatosensory hand representations revisited. Cerebral Cortex 2001;11(4):312–21. doi: 10.1093/cercor/11.4.312 11278194
37. Hlustik P, Solodkin A, Noll DC, Small SL. Cortical plasticity during three-week motor skill learning. Journal of Clinical Neurophysiology 2004;21(3):180–91. 15375348
38. Volkmann J, Schnitzler A, Witte OW, Freund H. Handedness and asymmetry of hand representation in human motor cortex. Journal of Neurophysiology 1998;79(4):2149–54. doi: 10.1152/jn.1998.79.4.2149 9535974
39. Yousry TA, Schmid UD, Alkadhi H, Schmidt D, Peraud A, Buettner A, et al. Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. Brain 1997;120(Pt 1):141–57.
40. Yusoff AN, Mohamad M, Hamid AIA, Abdullah W, Kamil WA, Hashim MH, et al. Functional specialisation and effective connectivity in cerebral motor cortices. Malaysian Journal of Medicine and Health Sciences 2010;6(2):71–92.
41. Bestmann S, Swayne O, Blankenburg F, Ruff CC, Haggard P, Weiskopf N, et al. Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cerebral cortex 2008;18(6):1281–1291. doi: 10.1093/cercor/bhm159 17965128
42. Beisteiner R, Gartus A, Erdler M, Mayer D, Lanzenberger R, Deecke L. Magnetoencephalography indicates finger motor somatotopy. European Journal of Neuroscience 2004;19(2):465–72. doi: 10.1111/j.1460-9568.2004.03115.x 14725641
43. Slobounov S, Chiang H, Johnston J, Ray W. Modulated cortical control of individual fingers in experienced musicians: an EEG study. Electroencephalographic study. Clinical Neurophysiology 2002;113(12):2013–24. 12464342
44. Qin S, Duan X, Supekar K, Chen H, Chen T, Menon V. Large-scale intrinsic functional network organization along the long axis of the human medial temporal lobe. Brain Structure and Function 2016;221(6):3237–3258. doi: 10.1007/s00429-015-1098-4 26336951
45. Igloi K, Doeller CF, Berthoz A, Rondi-Reig L, Burgess N. Lateralized human hippocampal activity predicts navigation based on sequence or place memory. Proceedings of the National Academy of Sciences 2010;107(32):14466–14471.
46. Miller J, Watrous AJ, Tsitsiklis M, Lee SA, Sheth SA, Schevon CA, et al. Lateralized hippocampal oscillations underlie distinct aspects of human spatial memory and navigation. Nature communications 2018;9(1):2423. doi: 10.1038/s41467-018-04847-9 29930307
47. Albouy G, Fogel S, King BR, Laventure S, Benali H, Karni A, et al. Maintaining vs. enhancing motor sequence memories: Respective roles of striatal and hippocampal systems. Neuroimage 2015;108:423–434. doi: 10.1016/j.neuroimage.2014.12.049 25542533
48. Albouy G, King BR, Maquet P, Doyon J. Hippocampus and striatum: Dynamics and interaction during acquisition and sleep-related motor sequence memory consolidation. Hippocampus 2013;23(11):985–1004. doi: 10.1002/hipo.22183 23929594
49. Balleine BW, O'Doherty JP. Human and Rodent Homologies in Action Control: Corticostriatal Determinants of Goal-Directed and Habitual Action. 2010.
50. Schwabe L. Stress and the engagement of multiple memory systems: integration of animal and human studies. Hippocampus 2013;23(11):1035–1043. doi: 10.1002/hipo.22175 23929780
51. Pignatelli M, Beyeler A, Leinekugel X. Neural circuits underlying the generation of theta oscillations. Journal of Physiology-Paris 2012;106(3):81–92.
52. Kober SE, Neuper C. Sex differences in human EEG theta oscillations during spatial navigation in virtual reality. International Journal of Psychophysiology 2011;79(3):347–355. doi: 10.1016/j.ijpsycho.2010.12.002 21146566
53. Cruikshank LC, Singhal A, Caplan JB. Theta oscillations reflect a putative neural mechanism for human sensorimotor integration. Journal of Neurophysiology 2012:jn. 00893.2010.
54. Barnett AJ, O'neil EB, Watson HC, Lee ACH. The human hippocampus is sensitive to the durations of events and intervals within a sequence. Neuropsychologia 2014;64:1–12. doi: 10.1016/j.neuropsychologia.2014.09.011 25223466
55. MacDonald CJ, Fortin NJ, Sakata S, Meck WH. Retrospective and prospective views on the role of the hippocampus in interval timing and memory for elapsed time. Timing & Time Perception 2014;2(1):51–61.
56. MacDonald CJ. Prospective and retrospective duration memory in the hippocampus: is time in the foreground or background? Phil. Trans. R. Soc. B 2014;369(1637):20120463. doi: 10.1098/rstb.2012.0463 24446497
57. Caplan JB, Madsen JR, Schulze-Bonhage A, Aschenbrenner-Scheibe R, Newman EL, Kahana MJ. Human θ oscillations related to sensorimotor integration and spatial learning. The Journal of neuroscience 2003;23(11):4726–4736. 12805312
58. Ekstrom AD, Watrous AJ. Multifaceted roles for low-frequency oscillations in bottom-up and top-down processing during navigation and memory. Neuroimage 2014;85:667–677. doi: 10.1016/j.neuroimage.2013.06.049 23792985
Článek vyšel v časopise
PLOS One
2019 Číslo 9
- S diagnostikou Parkinsonovy nemoci může nově pomoci AI nástroj pro hodnocení mrkacího reflexu
- Je libo čepici místo mozkového implantátu?
- Pomůže v budoucnu s triáží na pohotovostech umělá inteligence?
- AI může chirurgům poskytnout cenná data i zpětnou vazbu v reálném čase
- Nová metoda odlišení nádorové tkáně může zpřesnit resekci glioblastomů
Nejčtenější v tomto čísle
- Graviola (Annona muricata) attenuates behavioural alterations and testicular oxidative stress induced by streptozotocin in diabetic rats
- CH(II), a cerebroprotein hydrolysate, exhibits potential neuro-protective effect on Alzheimer’s disease
- Comparison between Aptima Assays (Hologic) and the Allplex STI Essential Assay (Seegene) for the diagnosis of Sexually transmitted infections
- Assessment of glucose-6-phosphate dehydrogenase activity using CareStart G6PD rapid diagnostic test and associated genetic variants in Plasmodium vivax malaria endemic setting in Mauritania
Zvyšte si kvalifikaci online z pohodlí domova
Všechny kurzy