Frequency specific spatial interactions in human electrocorticography: V1 alpha oscillations reflect surround suppression

Abstract

Electrical brain signals are often decomposed into frequency ranges that are implicated in different functions. Using subdural electrocorticography (ECoG, intracranial EEG) and functional magnetic resonance imaging (fMRI), we measured frequency spectra and BOLD responses in primary visual cortex (V1) and intraparietal sulcus (IPS). In V1 and IPS, 30–120 Hz (gamma, broadband) oscillations allowed population receptive field (pRF) reconstruction comparable to fMRI estimates. Lower frequencies, however, responded very differently in V1 and IPS. In V1, broadband activity extends down to 3 Hz. In the 4–7 Hz (theta) and 18–30 Hz (beta) ranges broadband activity increases power during stimulation within the pRF. However, V1 9–12 Hz (alpha) frequency oscillations showed a different time course. The broadband power here is exceeded by a frequency-specific power increase during stimulation of the area outside the pRF. As such, V1 alpha oscillations reflected surround suppression of the pRF, much like negative fMRI responses. They were consequently highly localized, depending on stimulus and pRF position, and independent between nearby electrodes. In IPS, all 3–25 Hz oscillations were strongest during baseline recording and correlated between nearby electrodes, consistent with large-scale disengagement. These findings demonstrate V1 alpha oscillations result from locally active functional processes and relate these alpha oscillations to negative fMRI signals. They highlight that similar oscillations in different areas reflect processes with different functional roles. However, both of these roles of alpha seem to reflect suppression of spiking activity.

Introduction

Electrical signals arising from synchronized human neural activity are characterized by components oscillating at different frequencies, associated with different aspects of neural processing. This oscillatory activity can result from cyclical interactions of excitatory and inhibitory pools of neurons, but this general description typically covers a large range of possible neural mechanisms (Ermentrout and Kopell, 1998, Jones et al., 2000, Kopell et al., 2000, Traub et al., 1996).

In particular, 9–12 Hz (alpha) oscillations, commonly recorded using electro- and magneto-encephalography (EEG and MEG), may be involved in functionally important computations within the local neural population (Cooper et al., 2003, Cooper et al., 2006, Jensen and Mazaheri, 2010, Palva et al., 2005a, Palva et al., 2005b) or may simply reflect large-scale disengagement of task-irrelevant areas (Klimesch, 1996, Klimesch et al., 2007, Pfurtscheller, 2001, Pfurtscheller, 2003, Ray and Cole, 1985). Computations within the local neural population suggest interactions with local neurons, while large-scale disengagement is likely to involve interactions with an inhibitory population in another part of the brain. Distinguishing between these possibilities is hindered by the low spatial resolution of recordings made outside the skull using EEG and MEG.

Here, we measure responses to visual stimuli using fMRI and electrocorticography (ECoG, intracranial EEG) in the same human subject. Both techniques have higher spatial resolution than EEG and MEG, and as such allow measurement of the aggregate neuronal receptive field within each recording site, the population receptive field (pRF) (Dumoulin and Wandell, 2008, Yoshor et al., 2007). We use pRF analysis to determine which stimulus positions elicit responses at the recording site. In early visual cortex, visual stimulation of areas outside the preferred visual field position of the neural population within an fMRI voxel causes decreases in BOLD fMRI signals (Logothetis, 2002, Tajima et al., 2010, Williams et al., 2003, Zenger-Landolt and Heeger, 2003), known as negative BOLD responses (NBR). The NBR are of neural origin (Shmuel et al., 2006, Smith et al., 2004a). Recently, we extended the pRF model to include suppressive surrounds that capture the NBR (Zuiderbaan et al., 2012). The pRF surround influences signals at the recording site comparably to the suppressive surround of classical RF responses seen in electrophysiology (Carandini, 2004, Cavanaugh et al., 2002, Fitzpatrick, 2000).

We demonstrate that measurements of neural oscillations show a clear signature of surround suppression at alpha frequencies in V1 in the absence of classical receptive field stimulation. This process is likely to be a major source of alpha activity measured on the scalp near the occipital pole. The high spatial resolution of ECoG allows us to measure the local components of this activity, and demonstrate that it is tightly localized. Low frequency oscillations in IPS, including alpha, are more broadband and less local, suggesting that they result from a different process, such as inter-area large-scale disengagement.