The spatially periodic activity of grid cells in the entorhinal cortex (EC) of the rodent, primate, and human provides a coordinate system that, together with the hippocampus, informs an individual of its location relative to the environment and encodes the memory of that location. Among the most defining features of grid-cell activity are the 60°rotational symmetry of grids and preservation of grid scale across environments. Grid cells, however, do display a limited degree of adaptation to environments. It remains unclear if this level of environment invariance generalizes to human grid-cell analogs, where the relative contribution of visual input to the multimodal sensory input of the EC is significantly larger than in rodents. Patients diagnosed with nontractable epilepsy who were implanted with entorhinal cortical electrodes performing virtual navigation tasks to memorized locations enabled us to investigate associations between grid-like patterns and environment. Here, we report that the activity of human entorhinal cortical neurons exhibits adaptive scaling in grid period, grid orientation, and rotational symmetry in close association with changes in environment size, shape, and visual cues, suggesting scale invariance of the frequency, rather than the wavelength, of spatially periodic activity. Our results demonstrate that neurons in the human EC represent space with an enhanced flexibility relative to neurons in rodents because they are endowed with adaptive scalability and context dependency.grid cell | spatial memory | entorhinal cortex | single unit | human
19The entorhinal cortex plays a vital role in our spatial awareness. Much focus has been placed on the spatial 20 activity of its individual neurons, which fire in a grid-like pattern across an environment 1 . On a population 21 level, however, neurons in the entorhinal cortex also display coherent rhythmic activity known as local field 22 potential. These local field oscillations have been shown to correlate with behavioural states but it remains 23 unclear how these oscillations relate to spatial behaviour and the spatial firing pattern of individual neurons. 24 To investigate this, we recorded entorhinal cortical neurons in the human brain during spatial memory tasks 25 performed in virtual environments. We observed a spatial modulation of the phase of action potentials relative 26 to the local field potentials. In addition, the spike phase modulation displayed correlation with the movement 27 of the avatar, displayed discrete phase tuning at the cellular level, rotated phase between electrodes, and 28 expressed spatially coherent phase maps that scaled with the virtual environment. Using surrogate data, we 29 demonstrated that spike phase coherence is dependent on the spatial phase dynamics of gamma oscillations. 30 We argue that the spatial coordination of spike generation with gamma rhythm underlies the emergence of 31 grid cell activity in the entorhinal cortex. These results shed a new light on the intricate interlacing between 32 the spiking activity of neurons and local field oscillations in the brain. 33 1 The medial entorhinal cortex (EC) is found in the medial temporal lobe of the mammalian brain and plays a 34 critical role in spatial awareness in rodents 1 as well as in humans [2][3][4] . The activity of grid cells and border cells 35 in the EC, together with place cells and head direction cells in the hippocampus and subiculum, respectively, 36 constitute key components of the allocentric navigation system enabling individuals to localize themselves 37 relative to the environment. The spatially periodic activity, a hallmark of grid cells 1 and displayed by about 38 50% in the human brain 4 , is hypothesized to support spatial navigation as an internal coordinate system. 39 In addition to their spatial tuning, EC neurons generate a broad frequency range of local field potentials 40 (LFPs) with two prominent harmonic components: theta and gamma 5 . Theta and gamma are predominant 41 in the rodent and human hippocampus and EC during active exploratory behaviour and REM-sleep 2,6 42 and hippocampal theta tend to phase-couple with slow gamma (30-50 Hz) from EC 7,8 . Theta-spike and 43 theta-gamma phase coherence are instrumental for memory encoding 9,10 . Although grid cells represent the 44 allocentric coordinate system for spatial navigation in a number of mammalian species 1,11,12 , the role of 45 oscillations in the generation of this spatially periodic activity is unknown. 46A grid of 16 extracellular microelectrodes ( Fig. 3a) was implanted in the EC of two human subjects...
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