Animal studies have shown robust electrophysiological activity in the sensory cortex in the absence of stimuli or tasks. Similarly, recent human functional magnetic resonance imaging (fMRI) revealed widespread, spontaneously emerging cortical fluctuations. However, it is unknown what neuronal dynamics underlie this spontaneous activity in the human brain. Here we studied this issue by combining bilateral single-unit, local field potentials (LFPs) and intracranial electrocorticography (ECoG) recordings in individuals undergoing clinical monitoring. We found slow (<0.1 Hz, following 1/f-like profiles) spontaneous fluctuations of neuronal activity with significant interhemispheric correlations. These fluctuations were evident mainly in neuronal firing rates and in gamma (40-100 Hz) LFP power modulations. Notably, the interhemispheric correlations were enhanced during rapid eye movement and stage 2 sleep. Multiple intracranial ECoG recordings revealed clear selectivity for functional networks in the spontaneous gamma LFP power modulations. Our results point to slow spontaneous modulations in firing rate and gamma LFP as the likely correlates of spontaneous fMRI fluctuations in the human sensory cortex.The neuronal events occurring in the sensory cortex when no stimulus is presented are not well understood. Contrary to traditional feed-forward models of information processing, a growing body of single-unit, LFP, electroencephalography (EEG), and optical imaging data point to robust levels of spontaneous neuronal activity in sensory areas of the mammalian cortex 1-7 . The modulation of such spontaneous neuronal activity can occur on very slow time scales 8, 9 . These robust spontaneous waves pose a challenge for models linking neuronal activity and sensory perception 10,11 , namely in explaining how the brain distinguishes between spontaneous events and vivid sensory percepts. One possibility is that the precise neuronal dynamics differ substantially between spontaneous and sensory-evoked conditions. This

SUMMARY Human recognition performance is characterized by abrupt changes in perceptual states. Understanding the neuronal dynamics underlying such transitions could provide important insights into mechanisms of recognition and perceptual awareness. Here we examined patients monitored for clinical purposes with multiple subdural electrodes. The patients participated in a backward masking experiment in which pictures of various object categories were presented briefly followed by a mask. We recorded ECoG from 445 electrodes placed in 11 patients. We found a striking increase in gamma power (30–70 Hz) and evoked responses specifically associated with successful recognition. The enhanced activation occurred 150–200 ms after stimulus onset and consistently outlasted the stimulus presentation. We propose that the gamma and evoked potential activations reflect a rapid increase in recurrent neuronal activity that plays a critical role in the emergence of a recognizable visual percept in conscious awareness.

The functional organization of human sensory cortex was studied by comparing intracranial EEG (iEEG) recordings of local field potentials in neurosurgical patients with functional magnetic resonance imaging (fMRI) obtained in healthy subjects. Using naturalistic movie stimuli, we found a tight correlation between these two measures throughout the human sensory cortex. Importantly, the correlation between the iEEG and fMRI signals was site-specific, exhibiting neuroanatomically specific coupling. In several cortical sites the iEEG activity was confined strictly to one object category. This site selectivity was not limited to faces but included other object categories such as houses and tools. The selectivity of the iEEG signals to images of different object categories was remarkably higher when compared with the selectivity of the corresponding fMRI signals. A plausible interpretation of the fMRI and iEEG results concerns cortical organization in which object categories are organized in a mosaic of narrowly tuned object-selective clusters.

Scalp electroencephalography and magnetoencephalography studies have revealed a rapid evoked potential "adaptation" where one visual stimulus suppresses the event-related potential (ERP) of the second stimulus. Here, we investigated a similar effect revealed in subdural intracranial recordings in humans. Our results show that the suppression of the subdural ERP is not associated with a reduction in the gamma frequency power, considered to reflect the underlying neural activity. Furthermore, the evoked potential suppression (EPS) phenomenon was not reflected in recognition behavior of the patients. Rather, the EPS was tightly linked to the level of gamma activity preceding the event, and this effect was independent of the interstimulus time interval. Analyzing other frequency bands failed to reveal a similar link. Our results thus show a consistent antagonism between subdural ERP and gamma power although both are considered markers for neural activity. We hypothesize that the ERP suppression is due to a desynchronization of neuronal firing resulting from recurrent neural activity in the vicinity of the freshly stimulated neurons and not an attenuation of the overall neural activity.

No abstract