Effect of Stimulus Intensity on the Spike–Local Field Potential Relationship in the Secondary Somatosensory Cortex

Abstract

Neuronal oscillations in the gamma frequency range have been reported in many cortical areas, but the role they play in cortical processing remains unclear. We tested a recently proposed hypothesis that the intensity of sensory input is coded in the timing of action potentials relative to the phase of gamma oscillations, thus converting amplitude information to a temporal code. We recorded spikes and local field potential (LFP) from secondary somatosensory (SII) cortex in awake monkeys while presenting a vibratory stimulus at different amplitudes. We developed a novel technique based on matching pursuit to study the interaction between the highly transient gamma oscillations and spikes with high time-frequency resolution. We found that spikes were weakly coupled to LFP oscillations in the gamma frequency range (40 -80 Hz), and strongly coupled to oscillations in higher gamma frequencies. However, the phase relationship of neither low-gamma nor high-gamma oscillations changed with stimulus intensity, even with a 10-fold increase. We conclude that, in SII, gamma oscillations are synchronized with spikes, but their phase does not vary with stimulus intensity. Furthermore, high-gamma oscillations (Ͼ60 Hz) appear to be closely linked to the occurrence of action potentials, suggesting that LFP high-gamma power could be a sensitive index of the population firing rate near the microelectrode.

The Subthreshold Relation between Cortical Local Field Potential and Neuronal Firing Unveiled by Intracellular Recordings in Awake Rats

“…In our experiments, the SD of the LFP signal, and the amplitude of LFP STA were in the 2-200 V range, compatible with previous studies (Eggermont and Smith, 1995;Fries et al, 2001;Pesaran et al, 2002;Goldberg et al, 2004;Poulet and Petersen, 2008;Ray et al, 2008;Nauhaus et al, 2009). First, we have compared the absolute peak amplitudes of LFP STA and of VmLFPcc, multiplied by the SD of the LFP signal.…”

“…For many questions having to do with cortical processing, it is imperative to examine the relationship between spikes and LFP rather than considering just the spikes or just the LFP (Gray and Singer, 1989;Eggermont and Smith, 1995;Steriade et al, 1996;Destexhe et al, 1999;Pesaran et al, 2002;Mehring et al, 2003;Henrie and Shapley, 2005;Rasch et al, 2008;Ray et al, 2008;Tiesinga et al, 2008;Xing et al, 2009). The typical measure used to correlate the activity of individual neurons to the LFP signal is the spike-triggered average (STA) of the field potential (Gray and Singer, 1989;Eggermont and Smith, 1995;Destexhe et al, 1999;Fries et al, 2001;Pesaran et al, 2002;Goldberg et al, 2004;Ray et al, 2008;Katzner et al, 2009;Nauhaus et al, 2009).…”

“…The typical measure used to correlate the activity of individual neurons to the LFP signal is the spike-triggered average (STA) of the field potential (Gray and Singer, 1989;Eggermont and Smith, 1995;Destexhe et al, 1999;Fries et al, 2001;Pesaran et al, 2002;Goldberg et al, 2004;Ray et al, 2008;Katzner et al, 2009;Nauhaus et al, 2009). In vivo, synaptic inputs to the cortical neurons are the primary cause for their membrane potential (V m ) fluctuations, responsible for spiking (Steriade, 2001), which is in particular evident from the synchrony of simultaneously recorded nearby neurons (Lampl et al, 1999;Hasenstaub et al, 2005;Volgushev et al, 2006;Okun and Lampl, 2008;Poulet and Petersen, 2008).…”

Rotating waves during human sleep spindles organize global patterns of activity that repeat precisely through the night

“…activity (Ray et al, 2008;Ray and Maunsell, 2011;Ray, 2015; similar in nature to the 'broadband power shift' described in Manning et al, 2009), consistently increases around spindles ( Figure 4A). Further, HGP is modulated by spindle phase ( Figure 4B), increasing towards the surface-positive (depth-negative) peak, consistent with previous animal (Peyrache et al, 2011) and human recordings.…”

Oscillations, Phase-of-Firing Coding, and Spike Timing-Dependent Plasticity: An Efficient Learning Scheme

“…For example, Montemurro et al (2008), Ray et al (2008), and Kayser et al (2009) all looked for it unsuccessfully [but see König et al (1995), Fries et al (2001), Hoffman et al (2009), andKoepsell et al (2009) for exceptions]. In the studies by Jacobs et al (2007) and Ray et al (2008), some spikes did lock to gamma oscillations, but the preferred phases always tended to be near the oscillation peaks, ruling out PoFC, but suggesting instead a binary code in which information would be coded in the combination of neurons which fire at least once in each oscillation cycle. Such a code could probably be decoded by STDP, but it is beyond the scope of this paper.…”