We identified four frequency components of EM-related LFP activity based on the time-frequency characteristics of the LFP modulations in the primary visual cortex of monkeys performing voluntary visual exploration of natural-scene images. The center frequencies of the four components were found in the delta-theta band (2–4 Hz), the alpha-beta band (10–13 Hz), the low-gamma band (20–40 Hz), and the high-gamma band (>100 Hz). The strongest changes in the LFP power in response to EMs were observed in the alpha-beta and the low-gamma band components, while the phase-locking to the timing of EMs was strongest in the delta-theta band component. We found positive correlations between the degree of phase-locking in the delta-theta band and the magnitude of the power increase after EMs in the other frequency bands. This correlation was strongest for the alpha-beta and the low-gamma band power.
The strongest phase-locking within the delta-theta band was observed at slightly different frequencies for different monkeys, but these frequencies systematically matched the individual saccade frequencies, i.e., the inverse of the median ISI. This result is consistent with a previous finding on the phase-locking of the delta-theta band LFP oscillations in V1 and V4 to the onset of micro-saccades during prolonged fixation (Bosman et al., 2009
). This consistency offers a strong support for the view that regular saccades and micro-saccades constitute a functional continuum of ocular movements that influence the visual cortex (Otero-Millan et al., 2008
; Hafed et al., 2009
). Our results about the delta-theta band phase-locking are also consistent with previous findings on the delta-theta band LFP phase during passive viewing of natural movies (Belitski et al., 2008
; Mazzoni et al., 2011
). These studies found that the LFP phase in this frequency band contains information about the slow fluctuations of the luminance of a presented movie. The authors argued “Because movies contain most power at low frequency, it is conceivable that some of the features for which LFPs are selective are characterized by slow fluctuations and thus are reflected in LFPs at low frequency” (Belitski et al., 2008
). We assert that, in natural vision, the temporal changes in the afferent input to the visual system on this time scale are caused by voluntary saccadic EMs, even if there are no movements in the external visual world. Thus, the phase-locking of the delta-theta band LFP oscillation in the present study is considered as an extension of the previous finding in passive movie viewing to the condition of active visual exploration.
The degree of the observed phase-locking in the delta-theta band was not homogeneous across different recording sites, but it was highly variable. We could not find any systematic relation between the strength of the phase-locking and (a rough estimate of) the recording depth within the cortical layers. This variability may be explained by the differences in the response properties of the local neuronal populations across V1 and/or the statistical properties of the natural image stimuli we used. An elucidation of this issue would require further experimentation.
Modulation of oscillatory power in relation to EMs was observed in the alpha-beta, the low-gamma, and the-high gamma frequency bands. The increase in power in the alpha-beta band is consistent with our previous results (Ito et al., 2011
). The power modulations in the low- and the high-gamma bands, and their temporal relation to that in the alpha-beta band are novel findings of the present study. The low-gamma component shares a common time course of power changes with the alpha-beta component, while the high-gamma component shows a clearly different time course in the changes than the others. The degree of the power changes is larger in the alpha-beta and the low-gamma bands than in the high-gamma band. The phases of the high- and the low-gamma components are not locked to the onset of EMs, which is a signature of induced oscillations, while the power increase in the alpha-beta component is associated with phase-locking, which is a signature of evoked oscillations. All these differences in response properties across different frequency components strongly suggest that the neuronal activity in V1 during active vision is composed of multiple oscillatory components which have different mechanisms of generation.
The peak values of the power in response to EMs showed a large variability across recording sites, as was also found for the ISPC of the delta-theta component. We found that the variability in the ISPC and the power were not independent, but show positive correlation between the delta-theta band ISPC and the power of the other frequency components derived from identical electrodes. This correlation was particularly strong for the alpha-beta and the low-gamma power. A parsimonious interpretation of this result is that the delta-theta, the alpha-beta, and the low-gamma components are just the reflections of an identical physiological process that possesses power in a wide frequency range (for example, evoked oscillatory activity with a non-sinusoidal waveform). However, the results of our saccade-duration resolved analysis argue against this view. We found that the delta-theta phase is locked more to fixation onset than to saccade onset, while the power of the alpha-beta and the low-gamma is locked more to saccade onset. This strongly suggests that there are at least two separate underlying neuronal processes that are related to the onset of fixations and that of saccades, and that the former is responsible for the generation of the delta-theta component and the latter for the other (the alpha-beta and the low-gamma) components. Furthermore, recent studies have shown that, while the power of the high-gamma broad band activity reflects the amount of the spiking activity of local neuronal pools, the power in lower frequencies is more related to network oscillations (Ray et al., 2008
; Ray and Maunsell, 2011
). We found that the phase-locking of the delta-theta component is more strongly correlated to the power of the low-gamma component than to the power of the high-gamma component. This suggests that the LFP activity in the delta-theta band is not a mere reflection of the changes in the spiking activity of the local neuronal pool, but it would be related to network oscillations of neuronal excitability.
As illustrated in Figure , the observed correlation between the phase-locking in the delta-theta band and the evoked power in the alpha-beta and the low-gamma bands can be interpreted as cross-frequency interactions occurring via the mechanism of PAC (Jensen and Colgin, 2007
; Canolty and Knight, 2010
). Our observations of the ISPC-power correlation can be explained as a reflection of PAC between the slow LFP oscillation at the saccade frequency and the fast-evoked LFP oscillations in the alpha-beta or the low-gamma frequency band. Under the assumption of such PAC, a recording with high delta-theta ISPC would be associated with strong alpha-beta or low-gamma power, since the enhancement of the alpha-beta or low-gamma amplitude at a proper delta-theta phase occurs at a consistent timing in relation to the timing of EM, which results in a high-evoked power on average across EMs (Figure left). On the other hand, if the delta-theta phase is not locked to the timing of EMs, such amplitude enhancement occurs at arbitrary timing and hence the average-evoked power becomes smaller compared to the case with strong phase-locking (Figure right). A possible mechanism underlying such cross-frequency interaction is, as proposed by Mazzoni et al. (2008
), a modulation of the baseline excitability of V1 neurons by unspecific slow cortical activity. In natural vision, such a slow activity could be a top-down, predictive signal entrained to the rhythmic EMs (Lakatos et al., 2008
), or could originate from the LGN activity that is rhythmically modulated by a corollary signal derived from the motor commands to the eye muscles (Wurtz et al., 2011
). Recent studies have reported the evidence that visual attention is temporally modulated at the theta band rhythm (Landau and Fries, 2012
) and that such modulation is mediated by cross-frequency interaction between the theta and the gamma band LFP activities (Bosman et al., 2012
). Since EMs are tightly related to visual attention (Corbetta et al., 1998
), the EM-related cross-frequency interaction between the delta-theta and the higher frequency components identified in the present study could be a candidate mechanism for modulation of attention during natural vision with voluntary EMs.
Previous studies on natural viewing have shown that firing rates of V1 neurons during exposure to complex scenes are characteristically low (Gallant et al., 1998
; Vinje and Gallant, 2000
; Olshausen and Field, 2005
; MacEvoy et al., 2008
; Maldonado et al., 2008
). For example, Maldonado et al. (2008
) reported that the peak firing rate during visual fixations is on average ~15 Hz. Under such a condition, rate coding, i.e., information coding by spike counts during an certain period, would be unreliable, since given the low firing rates the number of spikes within one fixation would be at most 3–5 spikes and hence any additional spontaneous spiking during a fixation period could considerably alter the information content. This perspective is also supported by theoretical and experimental works that have proposed that information may not be encoded solely in firing rates but also in the precise and coordinated timing of action potentials, such as in the response latency (Gawne et al., 1996
; Reich et al., 2001
; VanRullen and Thorpe, 2002
) or the spike timing in relation to background LFP oscillations (Montemurro et al., 2008
; Nadasdy, 2009
). We found in our previous studies that spike synchrony between V1 neurons exceeding chance synchrony predicted by the firing rates occurs and increases at around the onset of the rate change in response to visual fixation (Maldonado et al., 2008
). In Ito et al. (2011
) we additionally found that the first visually evoked spikes during fixations are locked to a specific phase of the LFP oscillations in the beta frequency band. Thus, the beta band LFP oscillations seem to provide a time-reference for spike synchrony among V1 neurons. Our present results suggest the enhancement of the alpha-beta power by phase-locking of the delta-theta oscillations to EMs. Taken together, these results point toward hierarchically organized brain activity in the temporal domain such that slower activities on the behavioral time scale influence the timing of single spikes via multiple levels of interaction between different time scales. Thus, experiments that employ voluntary, exploratory sensing behaviors by the animals provide the context for studying such temporal organization of neuronal activities and reveal the dynamic aspects of the sensory systems of the brain.