While driving, we make numerous conscious decisions such as route and turn direction selection. Although drivers are held responsible, the neural processes that govern such decisions are not clear. We recorded intracranial EEG signals from six patients engaged in a computer-based driving simulator. Patients decided which way to turn (left/right) and subsequently reported the time of the decision. We show that power modulations of gamma band oscillations (30–100 Hz) preceding the reported time of decision (up to 5.5 sec) allow prediction of decision content with high accuracy (up to 82.4%) on a trial-by-trial basis, irrespective of subsequent motor output. Moreover, these modulations exhibited a spatiotemporal gradient, differentiating left/right decisions earliest in premotor cortices and later in more anterior and lateral regions. Our results suggest a preconscious role for the premotor cortices in early stages of decision-making, which permits foreseeing and perhaps modifying the content of real-life human choices before they are consciously made.

The division of cortical visual processing into distinct dorsal and ventral streams is a key concept in primate neuroscience [Goodale, M. A., & Milner, A. D. Separate visual pathways for perception and action. Trends in Neurosciences, 15, 20–25, 1992; Steele, G., Weller, R., & Cusick, C. Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys. Journal of Comparative Neurology, 306, 495–520, 1991]. The ventral stream is usually characterized as a “What” pathway, whereas the dorsal stream is implied in mediating spatial perception (“Where”) and visually guided actions (“How”). A subpathway emerging from the dorsal stream and projecting to the medial-temporal lobe has been identified [Kravitz, D. J., Saleem, K. S., Baker, C. I., & Mishkin, M. A new neural framework for visuospatial processing. Nature Reviews Neuroscience, 12, 217–230, 2011; Cavada, C., & Goldman-Raiuc, P. S. Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory cortico-cortical connections. Journal of Comparative Neurology, 287, 393–421, 1989]. The current article studies the coordination of visual information typically associated with the dorsal stream (“Where”), with planned movements, focusing on the temporal lobe. We recorded extracellular activity from 565 cells in the human medial-temporal and frontal lobes while 13 patients performed cued hand movements with visual feedback (visuomotor task), without feedback (motor task), or observed visual feedback without motor movement (visual-only task). We discovered two different neural populations in the human medial-temporal lobe. One consists of motor-like neurons representing hand position, speed or acceleration during the motor task but not during the visuomotor or visual tasks. The other is specific to the parahippocampal gyrus (an area known to process visual motion [Gur, M., & Snodderly, D. M. Direction selectivity in V1 of alert monkeys: Evidence for parallel pathways for motion processing. Journal of Physiology, 585, 383–400, 2007; Sato, N., & Nakamura, K. Visual response properties of neurons in the parahippocampal cortex of monkeys. Journal of Neurophysiology, 90, 876–886, 2003]) and encodes speed, acceleration, or direction of hand movements, but only during the visuomotor task: neither during visual-only nor during motor tasks. These findings suggest a functional basis for the anatomical subpathway between the dorsal stream and the medial-temporal lobe. Similar to the recent expansion of the motor control process into the sensory cortex [Matyas, F., Sreenivasan, V., Marbach, F., Wacongne, C., Barsy, B., Mateo, C., et al. Motor control by sensory cortex. Science, 330, 1240–1243, 2010], our findings render the human medial-temporal lobe an important junction in the process of planning and execution of motor acts whether internally or externally (visually) driven. Thus, the medial-temporal lobe might serve as an integration node between the two processing streams. Our findings thus shed new light on the brain mechanisms underlying visuomotor coordination which is a crucial capacity for everyday survival, whether it is identifying and picking up food, sliding a key into a lock, driving a vehicle, or escaping a predator.

During spatial navigation, lesion and functional imaging studies suggest that the right hemisphere has a unique functional role. However, studies of direct human brain recordings have not reported interhemisphere differences in navigation-related oscillatory activity. We investigated this apparent discrepancy using intracranial electroencephalographic recordings from 24 neurosurgical patients playing a virtual taxi driver game. When patients were virtually moving in the game, brain oscillations at various frequencies increased in amplitude compared with periods of virtual stillness. Using log-linear analysis, we analyzed the region and frequency specificities of this pattern and found that neocortical movement-related gamma oscillations (34–54 Hz) were significantly lateralized to the right hemisphere, especially in posterior neocortex. We also observed a similar right lateralization of gamma oscillations related to searching for objects at unknown virtual locations. Thus, our results indicate that gamma oscillations in the right neocortex play a special role in human spatial navigation.

Local field potentials (LFPs) reflect the averaged dendrosomatic activity of synaptic signals of large neuronal populations. In this study, we investigate the selectivity of LFPs and single neuron activity to semantic categories of visual stimuli in the medial temporal lobe of nine neurosurgical patients implanted with intracranial depth electrodes for clinical reasons. Strong selectivity to the category of presented images was found for the amplitude of LFPs in 8% of implanted microelectrodes and for the firing rates of single and multiunits in 14% of microelectrodes. There was little overlap between the LFP- and spike-selective microelectrodes. Separate analysis of the power and phase of LFPs revealed that the mean phase was category-selective around the θ frequency range and that the power of the LFPs was category-selective for high frequencies around the γ rhythm. Of the 36 microelectrodes with amplitude-selective LFPs, 30 were found in the hippocampus. Finally, it was possible to readout information about the category of stimuli presented to the patients with both spikes and LFPs. Combining spiking and LFP activity enhanced the decoding accuracy in comparison with the accuracy obtained with each signal alone, especially for short time intervals.

Different structures within the medial-temporal lobe likely make distinct contributions to declarative memory. In particular, several current psychological and computational models of memory predict that the hippocampus and parahippocampal regions play different roles in the formation and retrieval of declarative memories [e.g., Norman, K. A., & O'Reilly, R. C. Modeling hippocampal and neocortical contributions to recognition memory: A complementary-learning systems approach. Psychological Review, 110 , 611–646, 2003]. Here, we examined the neuronal firing patterns in these two regions during recognition memory. Recording directly from neurons in humans, we find that cells in both regions respond to novel stimuli with an increase in firing (excitation). However, already on the second presentation of a stimulus, neurons in these regions show very different firing patterns. In the parahippocampal region there is dramatic decrease in the number of cells responding to the stimuli, whereas in the hippocampus there is recruitment of a large subset of neurons showing inhibitory (decrease from baseline firing) responses. These results suggest that inhibition is a mechanism used by cells in the human hippocampus to support sparse coding in mnemonic processing. The findings also provide further evidence for the division of labor in the medial-temporal lobe with respect to declarative memory processes.