Stimulus-Specific Adaptation Decreases the Coupling of Spikes to LFP Phase.

Mohsen Parto Dezfouli,Mohammad Reza Daliri,Mohammad Zarei,Mehran Jahed

doi:10.3389/fncir.2019.00044

Abstract

Stimulus repetition suppresses the neural activity in different sensory areas of the brain. This mechanism of so-called stimulus-specific adaptation (SSA) has been observed in both spiking activity and local field potential (LFP) responses. However, much remains to be known about the effect of SSA on the spike–LFP relation. In this study, we approached this issue by investigating the spike-phase coupling (SPC) in control and adapting paradigms. For the control paradigm, pure tones were presented in a random unbiased sequence. In the adapting paradigm, the same stimuli were presented in a random pattern but it was biased to an adapter stimulus. In fact, the adapter occupied 80% of the adapting sequence. During the tasks, LFP and multi-unit activity were recorded simultaneously from the primary auditory cortex of 15 anesthetized rats. To clarify the effect of adaptation on the relation between spike and LFP responses, the SPC of the adapter stimulus in these two paradigms was evaluated. Here, we employed phase locking value method for calculating the SPC. Our data show a strong coupling of spikes to LFP phase most prominently in beta band. This coupling was observed to decrease in the adapting condition compared to the control one. Importantly, we found that adaptation reduces spikes dominantly from the preferred phase of LFP in which spikes are more likely to be present there. As a result, the preferred phase of LFP may play a key role in coordinating neuronal spiking activity in neural adaptation mechanism. This finding is important for interpretation of the underlying neural mechanism of adaptation and also can be used in the context of the network and related connectivity models.

Highlights

The activity in the low-frequency bands of the local field potential (LFP) indicates the combination of neural activity across larger networks of neurons (Buzsáki and Draguhn, 2004)
Since we found the coupling of the spike to LFP phase in beta range, we focused our analyses within the beta band (13–30 Hz), but the frequencies up to 120 Hz were analyzed
This study reported that stimulus-specific adaptation (SSA) suppresses the spike to LFP phase coupling most prominently in beta range

Summary

Introduction

Neural synchrony/desynchrony has been targeted of many recent brain studies and has deeply influenced modern knowledge in various functions, such as sensory coding, decision making, working memory, and selective attention (Eckhorn and Obermueller, 1993; Baker et al, 1999; Cutsuridis and Hasselmo, 2011; Muthukumaraswamy, 2011; Li et al, 2014; Adaptation and SPCMendoza-Halliday et al, 2014; Ruff and Cohen, 2014; Fazlali et al, 2016; Ding et al, 2017; Bahmani et al, 2018; Johnson et al, 2018a,b). LFPs reflect the activity of a population of neurons based on spatially averaged synaptic activity (Buzsáki and Draguhn, 2004; Buzsáki et al, 2012; Jansen et al, 2014). They are continuous cyclic signals with various frequency bands. The high frequencies of the LFP such as low-gamma and high-gamma bands reflect higher local activity (Csicsvari et al, 2003; Liu and Newsome, 2006; Whittingstall and Logothetis, 2009)

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