Dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with Kallmann syndrome
In Kallmann syndrome (KS), the peculiar phenomenon of bimanual synkinesis or mirror movement (MM) has been associated with a spectral shift, from lower to higher frequencies, of the resting-state fMRI signal of the large-scale sensorimotor brain network (SMN). To possibly determine whether a similar...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-08-01
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| Series: | Frontiers in Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2022.971809/full |
| _version_ | 1817996815367143424 |
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| author | Federica Di Nardo Renzo Manara Antonietta Canna Francesca Trojsi Gianluca Velletrani Antonio Agostino Sinisi Mario Cirillo Gioacchino Tedeschi Fabrizio Esposito |
| author_facet | Federica Di Nardo Renzo Manara Antonietta Canna Francesca Trojsi Gianluca Velletrani Antonio Agostino Sinisi Mario Cirillo Gioacchino Tedeschi Fabrizio Esposito |
| author_sort | Federica Di Nardo |
| collection | DOAJ |
| description | In Kallmann syndrome (KS), the peculiar phenomenon of bimanual synkinesis or mirror movement (MM) has been associated with a spectral shift, from lower to higher frequencies, of the resting-state fMRI signal of the large-scale sensorimotor brain network (SMN). To possibly determine whether a similar frequency specificity exists across different functional connectivity SMN states, and to capture spontaneous transitions between them, we investigated the dynamic spectral changes of the SMN functional connectivity in KS patients with and without MM symptom. Brain MRI data were acquired at 3 Tesla in 39 KS patients (32 without MM, KSMM-, seven with MM, KSMM+) and 26 age- and sex-matched healthy control (HC) individuals. The imaging protocol included 20-min rs-fMRI scans enabling detailed spectro-temporal analyses of large-scale functional connectivity brain networks. Group independent component analysis was used to extract the SMN. A sliding window approach was used to extract the dynamic spectral power of the SMN functional connectivity within the canonical physiological frequency range of slow rs-fMRI signal fluctuations (0.01–0.25 Hz). K-means clustering was used to determine (and count) the most recurrent dynamic states of the SMN and detect the number of transitions between them. Two most recurrent states were identified, for which the spectral power peaked at a relatively lower (state 1) and higher (state 2) frequency. Compared to KS patients without MM and HC subjects, the SMN of KS patients with MM displayed significantly larger spectral power changes in the slow 3 canonical sub-band (0.073–0.198 Hz) and significantly fewer transitions between state 1 (less recurrent) and state 2 (more recurrent). These findings demonstrate that the presence of MM in KS patients is associated with reduced spontaneous transitions of the SMN between dynamic functional connectivity states and a higher recurrence and an increased spectral power change of the high-frequency state. These results provide novel information about the large-scale brain functional dynamics that could help to understand the pathologic mechanisms of bimanual synkinesis in KS syndrome and, potentially, other neurological disorders where MM may also occur. |
| first_indexed | 2024-04-14T02:27:49Z |
| format | Article |
| id | doaj.art-7060ef1cae894065938f741c2fef44ed |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-04-14T02:27:49Z |
| publishDate | 2022-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Neuroscience |
| spelling | doaj.art-7060ef1cae894065938f741c2fef44ed2022-12-22T02:17:48ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2022-08-011610.3389/fnins.2022.971809971809Dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with Kallmann syndromeFederica Di Nardo0Renzo Manara1Antonietta Canna2Francesca Trojsi3Gianluca Velletrani4Antonio Agostino Sinisi5Mario Cirillo6Gioacchino Tedeschi7Fabrizio Esposito8Department of Advanced Medical and Surgical Sciences, University of Campania “Luigi Vanvitelli,”Naples, ItalyDepartment of Neuroscience, University of Padova, Padova, ItalyDepartment of Advanced Medical and Surgical Sciences, University of Campania “Luigi Vanvitelli,”Naples, ItalyDepartment of Advanced Medical and Surgical Sciences, University of Campania “Luigi Vanvitelli,”Naples, ItalyDepartment of Medicine, Surgery and Dentistry, University of Salerno, Salerno, ItalyDepartment of Advanced Medical and Surgical Sciences, University of Campania “Luigi Vanvitelli,”Naples, ItalyDepartment of Advanced Medical and Surgical Sciences, University of Campania “Luigi Vanvitelli,”Naples, ItalyDepartment of Advanced Medical and Surgical Sciences, University of Campania “Luigi Vanvitelli,”Naples, ItalyDepartment of Advanced Medical and Surgical Sciences, University of Campania “Luigi Vanvitelli,”Naples, ItalyIn Kallmann syndrome (KS), the peculiar phenomenon of bimanual synkinesis or mirror movement (MM) has been associated with a spectral shift, from lower to higher frequencies, of the resting-state fMRI signal of the large-scale sensorimotor brain network (SMN). To possibly determine whether a similar frequency specificity exists across different functional connectivity SMN states, and to capture spontaneous transitions between them, we investigated the dynamic spectral changes of the SMN functional connectivity in KS patients with and without MM symptom. Brain MRI data were acquired at 3 Tesla in 39 KS patients (32 without MM, KSMM-, seven with MM, KSMM+) and 26 age- and sex-matched healthy control (HC) individuals. The imaging protocol included 20-min rs-fMRI scans enabling detailed spectro-temporal analyses of large-scale functional connectivity brain networks. Group independent component analysis was used to extract the SMN. A sliding window approach was used to extract the dynamic spectral power of the SMN functional connectivity within the canonical physiological frequency range of slow rs-fMRI signal fluctuations (0.01–0.25 Hz). K-means clustering was used to determine (and count) the most recurrent dynamic states of the SMN and detect the number of transitions between them. Two most recurrent states were identified, for which the spectral power peaked at a relatively lower (state 1) and higher (state 2) frequency. Compared to KS patients without MM and HC subjects, the SMN of KS patients with MM displayed significantly larger spectral power changes in the slow 3 canonical sub-band (0.073–0.198 Hz) and significantly fewer transitions between state 1 (less recurrent) and state 2 (more recurrent). These findings demonstrate that the presence of MM in KS patients is associated with reduced spontaneous transitions of the SMN between dynamic functional connectivity states and a higher recurrence and an increased spectral power change of the high-frequency state. These results provide novel information about the large-scale brain functional dynamics that could help to understand the pathologic mechanisms of bimanual synkinesis in KS syndrome and, potentially, other neurological disorders where MM may also occur.https://www.frontiersin.org/articles/10.3389/fnins.2022.971809/fullKallmann syndromemirror movementsdynamic functional connectivitysensorimotor networkK-meansconnectivity states |
| spellingShingle | Federica Di Nardo Renzo Manara Antonietta Canna Francesca Trojsi Gianluca Velletrani Antonio Agostino Sinisi Mario Cirillo Gioacchino Tedeschi Fabrizio Esposito Dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with Kallmann syndrome Frontiers in Neuroscience Kallmann syndrome mirror movements dynamic functional connectivity sensorimotor network K-means connectivity states |
| title | Dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with Kallmann syndrome |
| title_full | Dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with Kallmann syndrome |
| title_fullStr | Dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with Kallmann syndrome |
| title_full_unstemmed | Dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with Kallmann syndrome |
| title_short | Dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with Kallmann syndrome |
| title_sort | dynamic spectral signatures of mirror movements in the sensorimotor functional connectivity network of patients with kallmann syndrome |
| topic | Kallmann syndrome mirror movements dynamic functional connectivity sensorimotor network K-means connectivity states |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2022.971809/full |
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