Effects of different transcranial direct current stimulation protocols on visuo-spatial contextual learning formation: evidence of homeostatic regulatory mechanisms

Abstract

In the present study we tested the effects of different transcranial direct current stimulation (tDCS) protocols in the formation of visuo-spatial contextual learning (VSCL). The study comprised three experiments designed to evaluate tDCS-induced changes in VSCL measures collected during the execution of a visual search task widely used to examine statistical learning in the visuo-spatial domain. In Experiment 1, we probed for the effects of left-posterior parietal cortex (PPC) anodal-tDCS (AtDCS) at different timings (i.e. offline and online) and intensities (i.e. 3 mA and 1.5 mA). The protocol producing the more robust effect in Experiment 1 was used in Experiment 2 over the right-PPC, while in Experiment 3, cathodal-tDCS (CtDCS) was applied over the left-PPC only at a high intensity (i.e. 3 mA) but varying timing of application (offline and online). Results revealed that high intensity offline AtDCS reduced VSCL regardless of the stimulation side (Experiment 1 and 2), while no significant behavioral changes were produced by both online AtDCS protocols (Experiment 1) and offline/online CtDCS (Experiment 3). The reduced VSCL could result from homeostatic regulatory mechanisms hindering normal task-related neuroplastic phenomena. Transcranial electrical stimulation (tES) is a non-invasive brain stimulation technique extensively used in cognitive neuroscience to produce transient modifications of brain activity. Among the various existing tES protocols, transcranial direct current stimulation (tDCS) is doubtless the most known and a wealth of works have demonstrated its capability to modulate neural responses and to shape behaviour 1-4. It consists in the application of weak direct electrical currents (mostly, 1 or 2 mA) for a few minutes (usually not more than 30 minutes) via a pair of electrodes positioned on the scalp. The electrical field generated by the current is capable to modulate membrane permeability and post-synaptic neuronal activity in both excitatory and inhibitory fashion. Because of single neuron registrations, we know that anodal-tDCS (AtDCS) induces an increase (depolarization) and cathodal-tDCS (CtDCS) causes a decrease (hyperpolarization) in permeability of the of neuronal membrane potential of stimulated neurons 5,6. In the long run (i.e., after effects), the two processes are thought to promote neuroplasticity through the induction of long-term potentiation (LTP) and long-term depression (LTD)-like effects 1,7-9. At the behavioural level, using the stimulation-dependent model, it is generally expected that AtDCS applied during the execution of a task leads to enhanced behavioural performances on the task while the opposite is expected for CtDCS. These assumptions are primarily related to the abovementioned effects of tDCS on membrane permeability. Nevertheless, this model directly and simplistically associates the effects at the neuronal level to the effects at the behavioural level. Moreover, this description clearly represents an approximation mainly assuming the brain as a passive system....

tDCS over posterior parietal cortex increases cortical excitability but decreases learning: An ERPs and TMS-EEG study

“…Considering previous evidence which highlights the crucial role of timing in tDCS-learning interactions (Fricke et al, 2011;Pirulli et al, 2013;Roth-Alpermann et al, 2006), it is unlikely that the P2 increase and VSCL decrease that we observed are mere by-products of the stimulation alone, but rather reflect the interaction between offline 3 mA AtDCS induced effects and the following task-related cortical activation. This interpretation is supported by results obtained in our previous work where we showed that online (rather than offline) application of the same AtDCS protocol did not produce such a detrimental effect on behaviour (Grasso et al, 2020).…”

“…In the present study, we appraised the neurophysiological effects caused by the interaction of AtDCS and VSCL. In a previous work we showed that 3 mA AtDCS applied on PPC before the execution of a VSCL paradigm reduced the participants' ability to learn visuo-spatial configurations of stimuli (Grasso et al, 2020). Behavioural data from the present study confirmed the AtDCSmediated reduction of VSCL.…”

“…Investigating these topics in cortical regions involving a more distributed network of connections is crucial for a deeper understanding of tDCS-brain interactions when complex circuitries are involved. We recently showed that applying 3 mA offline AtDCS over posterior parietal cortex (PPC) produces a significant reduction of visuospatial contextual learning (VSCL) formation (Grasso et al, 2020). The paradigm used has been classically administered to investigate implicit statistical learning within the visuo-spatial domain and consists of a visual search task in which half of the search arrays are repeated across blocks (Chun & Jiang, 1998).…”

Visual P2p component responds to perceived numerosity

“…Furthermore, also our results suggest that numerosity adaptation likely affects cortical areas located within a relatively high hierarchical node while leaves activity within earlier cortical regions mostly unchanged. This is because while early component of the visual ERP response have been mostly associated with activity arising from striate or early extrastriate regions ( Di Russo et al, 2002 ), the P2p component was found to originate from the parietal cortex ( Hyde and Spelke, 2012 ; Fornaciai et al, 2017 ) and its amplitude was found to vary when low electrical current are applied over posterior parietal cortex ( Grasso et al, 2020b , 2021c ). Finally, we recently showed that numerosity adaptation is selective to salient features, such as color, suggesting that adaptation to numerical quantities likely occurs after feature-binding and other processing contributing to object recognition ( Grasso et al, 2022 ).…”

Transcranial Direct Current Stimulation and Cognition in Neuropsychiatric Disorders: Systematic Review of the Evidence and Future Directions

“…The possibility for double blinding allows for a more rigorous evaluation of the after-effects induced by active stimulation (Gandiga and others 2006). Although the exact mechanism of action of tDCS is still debated, the current triggers a dynamic adaptation of the threshold potential, increasing the probability that the synaptic input will generate a response in output neurons (Grasso and others 2020; Orlov and others 2017a). Importantly, it has been shown that tDCS effects can persist beyond the period of stimulation (Kuo and others 2008; Nitsche and others 2003; Nitsche and Paulus 2000, 2001), and that such long-term effects are likely mediated by changes in N -methyl- d -aspartate (NMDA) and GABA receptors activity, resulting in modulation of neural plasticity (Kuo and others 2014) (Fig.…”