Investigating neural correlates of conscious perception by frequency-tagged neuromagnetic responses

Abstract

In binocular rivalry, a subject views two incongruent stimuli through each eye but consciously perceives only one stimulus at a time, with a switch in perceptual dominance every few seconds. To investigate the neural correlates of perceptual dominance in humans, seven subjects were recorded with a 148-channel magnetoencephalography array while experiencing binocular rivalry. A red vertical grating f lickering at one frequency was presented to one eye through a red filter and a blue horizontal grating f lickering at a different frequency was presented to the other eye through a blue filter. Steady-state neuromagnetic responses at the two frequencies were used as tags for the two stimuli and analyzed with high-resolution power spectra. It was found that a large number of channels showed peaks at both frequencies, arranged in a horseshoe pattern from posterior to anterior regions, whether or not the subject was consciously perceiving the corresponding stimulus. However, the amount of power at the stimulus frequency was modulated in relation to perceptual dominance, being lower in many channels by 50-85% when the subject was not conscious of that stimulus. Binocular rivalry is a useful experimental paradigm for identifying aspects of neural activity that are correlated with conscious experience (1, 2). If two incongruent visual stimuli are simultaneously presented one through each eye, only one stimulus at a time is consciously perceived, and the two percepts alternate every few seconds. It was thought initially that rivalry might reflect competition between monocular neurons in primary visual cortex or at earlier stages. However, recent psychophysical studies have demonstrated that perceptual rivalry can occur even when both stimuli are presented through the same eye or when they are alternated between the eyes (2). Furthermore, single-unit recordings during binocular rivalry in monkeys indicate that, while the firing of most neurons in primary visual cortex correlates with the stimulus but not with the percept (3), the firing of cortical units in higher visual areas, such as inferior temporal cortex and superior temporal sulcus (4), is highly correlated with the visual percept.Human subjects are the referent of choice for investigating conscious perception (5). However, brain activity associated with rivalry is difficult to study in humans with techniques such as positron emission tomography and functional MRI because of their limited temporal resolution. Unit recordings, on the other hand, while offering high temporal resolution as well as neuronal specificity, are typically performed in overtrained animals and are not practical for providing global coverage of neural responses. At the expense of spatial resolution, magnetoencephalograms (MEGs) and electroencephalograms (EEGs) offer the advantage of high temporal resolution and reflect the synchronous activity of large populations of neurons (6, 7). In this study, we made use of a 148-channel MEG array to compare whole-head, steady-state-evoked responses ...

Natural Frequencies of Human Corticothalamic Circuits

“…However, steady-state responses, as other responses evoked by the stimulation of peripheral receptors, can only probe a limited set of primary sensory cortices. Moreover, they assess the tuning of corticothalamic circuits only indirectly, since they can be significantly affected by the bandwidth of peripheral receptors (Abraham and Alpern, 1984) by sensory gating (Emerson et al, 1988), attention levels (Hillyard et al, 1997), and stimulus perception (Tononi et al, 1998;Cosmelli et al, 2004).…”

Early Neural Correlates of Conscious Somatosensory Perception

“…Indeed, ␥-frequency-band phase synchrony in the primary somatosensory cortex is enhanced at ϳ200 ms after the onsets of consciously perceived somatosensory stimuli (Meador et al, 2002). Moreover, studies on binocular rivalry have shown that strengthened local (Fries et al, 1997) and largescale (Tononi et al, 1998;Srinivasan et al, 1999) neuronal synchrony is correlated with conscious stimulus perception, hence emphasizing the role of neuronal phase relationships in sensory awareness.…”

Modulating the Rate and Rhythmicity of Perceptual Rivalry Alternations with the Mixed 5-HT2A and 5-HT1A Agonist Psilocybin

“…Under these conditions, the observer will experience alternations between awareness and suppression of the two 'rivaling' images. Currently, the debate is focused on the relative influences of early vs late visual processes (Blake and Logothetis, 2002), with the majority of research using a variety of imaging (Kleinschmidt et al, 1998;Tong and Engel, 2001) and recording (Leopold and Logothetis, 1996;Tononi et al, 1998) techniques aimed at identifying the location and nature of neuronal activity that 'correlates' with perceptual awareness and suppression. Relatively little has been done, however, to investigate either the nature of the 'switch' that drives the alternations in visual awareness or the pharmacology underlying the rivalry process.…”