Slow-frequency TMS over the vermis impairs motion detection. A preliminary study on the lasting effects of cerebellar TMS over behavior
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1
University Milano Bicocca, Department of Psychology, Italy
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2
University of Pavia, Department of Brain and Behavioral Sciences, Italy
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3
National Neurological Institute C. Mondino, Brain Connectivity Center, Italy
Introduction
The proposal that the cerebellum is directly and primarily involved in coordinating movement has been the dominant theory of cerebellar function since the eighteenth century. Recently, new prospective on a possible role of the cerebellum in coordinating sensory data have been proposed in the motor domain (Manto et al., 2012) and in the cognitive domain, as well (e.g., Koziol et al., 2014). In particular, lesion studies showed that cerebellar patients are impaired in motion perception tasks (Jokisch et al., 2005; Nawrot & Rizzo, 1998). However, inconsistent evidence exists relatively to the topographic contribution of the cerebellum to this function, with some lesion studies pointing to the midline structures but not to cerebellar hemispheres (Nawrot & Rizzo, 1995, 1998) and others pointing also to the lateral parts of the cerebellum (Jokisch et al., 2005). Neuroimaging is also inconsistent: Dupont et al.(1994) found vermal activity in response to moving dot patterns and Baumann and Mattingley (2010) observed a complex pattern of activation in the cerebellar hemispheres. A recent neuro-stimulation study contributed to shed light on this controversy, showing that motion perception predominantly taps on the vermis (Cattaneo et al., 2014). Specifically, the authors applied on-line transcranial magnetic stimulation (TMS) while participants had to indicate the direction of moving dots and found lower performances when TMS was delivered on the vermis but not on the left or on the right cerebellar hemisphere. The aim of the present study is to extend prior evidence relative to the contribution of the vermis to motion perception, by employing more complex stimuli. In fact, lesion, neuroimaging and neuro-stimulation studies conducted so far focused mainly on horizontal movements (dots moving leftward and rightward, e.g., Baumann & Mattingley, 2010), and no investigation has been conducted on the role of the vermis in underpinning the perception of downward and upward dots movements. Moreover, we decided to use an offline paradigm, where TMS is delivered before participants perform the task, while in on-line paradigms (as the one adopted by Cattaneo et al., 2014) TMS is delivered during the task execution. Offline paradigms enable to test whether behavioral changes due to the TMS over the cerebellum outlast stimulation’s duration, thus opening new perspectives on the potential use of TMS as hypothetical rehabilitative tool.
Methods
18 healthy right-handed volunteers (3M, mean age=23.3 ys, S.D.=1.7) took part in the experiment.
Stimuli consisted of 100 white dots (one pixel each), placed at random positions within an imaginary square that subtended 4.3 x 4.3 of visual angle. A percentage of the 100 dots moved coherently (in one of four directions: rightward, leftward, upward or downward) and the remaining dots moved randomly. The ratio of coherent vs. random moving dots necessary to obtain a stable performance around 75% accuracy was determined at the beginning of the experiment for each subject by mean a thresholding procedure. Participants were instructed to report whether the visual stimulus moved leftward, rightward, upward or downward by key pressing (there were 4 response keys). Each block consisted in 80 trials (20 trials for each directions) presented in a random order. Figure 1 shows an example of the experimental trial. Each subject took part in three different experimental sessions, each corresponding to a TMS site: the cerebellar vermis, the primary visual cortex (V1) and the vertex (control site), localized by mean of a neuro-navigation system. Offline 1 Hz TMS (at 100% of the motor threshold) was administered for 15 minutes and participants performed the task twice: once before and once after receiving TMS.
Results
A repeated-measures ANOVA with as within-subjects factors Direction (horizontal axis vs. vertical axis), Session (preTMS vs. postTMS) and TMS site (vermis, V1 and vertex) was performed on accuracy rates and response times (RT).
The ANOVA on accuracy revealed neither a significant main effect Direction (p=.08), Session (p=.20), or TMS (p=.45). The interaction TMS by Session was significant, F(2,34)=3.43, p=.044, indicating that during vertex TMS participants performed better in the postTMS compared to the preTMS, t(17)=2.34, p=.032, reflecting learning effects. This was not the case of cerebellar TMS and V1 TMS, where accuracy rates were comparable between preTMS and postTMS sessions t(17)=10, p=.92, and t(17)<1, p=.69, respectively (see Figure 2). No other interactions reached significance (ps<.20).
The ANOVA on RT revealed a main effect of Direction, F(1,17)=15.87, p=.001, indicating that participants were faster in identifying movements on the horizontal axis compared to the vertical axis. The main effect of Session was also significant, F(1,17)=10.60, p=.005, suggesting that participants were overall faster in the postTMS compared to the preTMS sessions, reflecting learning effects. No other main effects or interactions were significant (ps>.16).
Discussion
In the present study we asked participants to perform a visual motion discrimination task before and after TMS was delivered over the cerebellar vermis, V1 and the vertex (control condition). TMS applied over the vermis significantly impaired participants’ performance, similarly to TMS over V1. These results perfectly parallels the results of Cattaneo et al. (2014), corroborating previous findings on the causal role of the vermis in motion perception. Interestingly, we found that the detrimental effects of the TMS over the cerebellum were comparable when participants were required to discriminate dots moving on the horizontal axis and on the vertical axis, indicating that the cerebellum might have a general role in underpinning motion perception and discrimination. Finally, our results our results support the possible employment of TMS as a tool to promote changes in the brain activity paralleled by behavioral modifications able to overcome the exact time of the stimulation. Future researches need to be carried out in order to complement these findings, specifically testing whether high frequency (vs. low frequency) cerebellar TMS can improved (rather than impair) motion perception abilities both in healthy participants and patients
References
Baumann O, Mattingley JB: Scaling of neural responses to visual and auditory motion in the human cerebellum. J Neurosci 2010, 30: 4489-4495.
Cattaneo Z, Renzi C, Casali S, Silvanto J, Vecchi T, Papagno C, D'Angelo E: Cerebellar vermis plays a causal role in visual motion discrimination. Cortex 2014, 58: 272-280.
Dupont P, Orban GA, De Bruyn B, Verbruggen A, Mortelmans L: Many areas in the human brain respond to visual motion. J Neurophysiol 1994, 72: 1420-1424.
Jokisch D, Troje NF, Koch B, Schwarz M, Daum I: Differential involvement of the cerebellum in biological and coherent motion perception. Eur J Neurosci 2005, 21: 3439-3446.
Koziol LF, Budding D, Andreasen N, D’Arrigo S, Bulgheroni S, Imamizu H, Pezzulo G: Consensus paper: the cerebellum's role in movement and cognition. Cerebellum 2014, 13: 151-177.
Manto M, Bower JM, Conforto AB, Delgado-García JM, da Guarda SNF, Gerwig M, Molinari M: Consensus paper: roles of the cerebellum in motor control—the diversity of ideas on cerebellar involvement in movement. Cerebellum 2012, 11: 457-487.
Nawrot M, Rizzo M: Chronic motion perception deficits from midline cerebellar lesions in human. Vision Res 1998, 38: 2219-2224.
Keywords:
TMS,
Cerebellum,
Motion Perception,
Vermis,
slow frequency TMS
Conference:
The Cerebellum inside out: cells, circuits and functions
, ERICE (Trapani), Italy, 1 Dec - 5 Dec, 2016.
Presentation Type:
poster
Topic:
Integrative nuroscience and MRI
Citation:
Ferrari
C,
Oldrati
V,
Reverberi
C,
Vecchi
T and
Cattaneo
Z
(2019). Slow-frequency TMS over the vermis impairs motion detection. A preliminary study on the lasting effects of cerebellar TMS over behavior.
Conference Abstract:
The Cerebellum inside out: cells, circuits and functions
.
doi: 10.3389/conf.fncel.2017.37.000016
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Received:
30 Nov 2016;
Published Online:
25 Jan 2019.
*
Correspondence:
PhD. Chiara Ferrari, University Milano Bicocca, Department of Psychology, Milano, MI, Italy, Chiara.ferrari@unipv.it