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Gardner, R. J.

Publications and source records attributed to Gardner, R. J..

6 recordsLinked to original sources

Left-right-alternating theta sweeps in the entorhinal-hippocampal spatial map

Place cells in the hippocampus and grid cells in the entorhinal cortex are elements of a neural map of self-position1-5. To benefit navigation, this representation must be dynamically related to surrounding locations2. A candidate mechanism for linking places along an animals path has been described in place cells, where the sequence of spikes within each cycle of the hippocampal theta oscillation encodes a trajectory from the animals current location towards upcoming locations6-8. In mazes that bifurcate, such trajectories alternately traverse the two upcoming arms as the animal approaches the choice point9,10, raising the possibility that the trajectories express available forward paths encoded on previous trials10. However, to bridge the animals path with the wider environment, beyond places previously or subsequently visited, an experience-independent spatial sampling mechanism might be required. Here we show in freely moving rats, that within individual theta cycles, ensembles of grid cells and place cells encode a position signal that sweeps linearly outwards from the animals location into the ambient environment, with sweep direction alternating stereotypically between left and right across successive theta cycles. These sweeps were accompanied by, and aligned with, a similarly alternating directional signal in a discrete population of parasubiculum cells with putative connections to grid cells via conjunctive gridxdirection cells. Sweeps extended into never-visited locations that were inaccessible to the animal and persisted during REM sleep. Sweep directions could be explained by an algorithm that maximizes cumulative coverage of surrounding space. The sustained and unconditional expression of theta-patterned left-right-alternating sweeps in the entorhinal-hippocampal positioning system provides an efficient look-around mechanism for sampling locations beyond the travelled path.

neuroscience↗

Grid-cell modules remain coordinated when neural activity is dissociated from external sensory cues

The representation of an animals position in the medial entorhinal cortex (MEC) is distributed across several modules of grid cells, each characterized by a distinct spatial scale. The population activity within each module is tightly coordinated and preserved across environments and behavioral states. Little is known, however, about the coordination of activity patterns across modules. We analyzed the joint activity patterns of hundreds of grid cells simultaneously recorded in animals that were foraging either in the light, when sensory cues could stabilize the representation, or in darkness, when such stabilization was disrupted. We found that the states of different grid modules are tightly coordinated, even in darkness, when the internal representation of position within the MEC deviates substantially from the true position of the animal. These findings suggest that internal brain mechanisms dynamically coordinate the representation of position in different modules, to ensure that grid cells jointly encode a coherent and smooth trajectory of the animal.

neuroscience↗

Toroidal topology of population activity in grid cells

The medial entorhinal cortex (MEC) is part of a neural system for mapping a subjects position within a physical environment1,2. Grid cells, a key component of this system, fire in a characteristic hexagonal pattern of locations3, and are organized in modules4,5 which collectively form a population code for the animals allocentric position1,6-8. The invariance of the correlation structure of this population code across environments9,10 and behavioural states11,12, independently of specific sensory inputs, has pointed to intrinsic, recurrently connected continuous attractor networks (CANs) as a possible substrate of the grid pattern1,2,13-16. However, whether grid cell networks show continuous attractor dynamics, and how they interface with inputs from the environment, has remained elusive due to the small samples of cells obtained to date. Here we show, with simultaneous recordings from many hundreds of grid cells, and subsequent topological data analysis, that the joint activity of grid cells from an individual module resides on a toroidal manifold, as expected in a two-dimensional CAN. Positions on the torus correspond to the moving animals position in the environment. Individual cells are preferentially active at singular positions on the torus. Their positions are maintained, with minimal distortion, between environments and from wakefulness to sleep, as predicted by CAN models for grid cells but not by alternative feed-forward models where grid patterns are created from external inputs by Hebbian plasticity17-22. This demonstration of network dynamics on a toroidal manifold provides the first population-level visualization of CAN dynamics in grid cells.

neuroscience↗

Neuropixels 2.0: A miniaturized high-density probe for stable, long-term brain recordings

To study the dynamics of neural processing across timescales, we require the ability to follow the spiking of thousands of individually separable neurons over weeks and months, during unrestrained behavior. To address this need, we introduce the Neuropixels 2.0 probe together with novel analysis algorithms. The new probe has over 5,000 sites and is miniaturized such that two probes plus a headstage, recording 768 sites at once, weigh just over 1 g, suitable for implanting chronically in small mammals. Recordings with high quality signals persisting for at least two months were reliably obtained in two species and six different labs. Improved site density and arrangement combined with new data processing methods enable automatic post-hoc stabilization of data despite brain movements during behavior and across days, allowing recording from the same neurons in the mouse visual cortex for over 2 months. Additionally, an optional configuration allows for recording from multiple sites per available channel, with a penalty to signal-to-noise ratio. These probes and algorithms enable stable recordings from >10,000 sites during free behavior in small animals such as mice.

neuroscience↗

Task-dependent mixed selectivity in the subiculum

CA1 and subiculum (SUB) connect the hippocampus to numerous output regions. Cells in both areas have place-specific firing fields, although they are more dispersed in SUB. Weak responses to head direction and running speed have been reported in both regions. However, how such information is encoded in CA1 and SUB, and the resulting impact on downstream targets, is poorly understood. Here we estimate the tuning of simultaneously recorded CA1 and SUB cells to position, head direction, and speed. Individual neurons respond conjunctively to these covariates in both regions but the degree of mixed representation is stronger in SUB, and more so during goal-directed spatial navigation than free foraging. Each navigational variable could be decoded with higher precision, from a similar number of neurons, in SUB than CA1. The findings point to a possible contribution of mixed-selective coding in SUB to efficient transmission of hippocampal representations to widespread brain regions.

neuroscience↗

Correlation structure of grid cells is preserved during sleep

The network of grid cells in the medial entorhinal cortex forms a fixed reference frame for mapping physical space. The mechanistic origin of the grid representation is unknown, but continuous attractor network (CAN) models explain multiple fundamental features of grid-cell activity. An untested prediction of CAN grid models is that the grid-cell network should exhibit an activity correlation structure that transcends behavioural or brain states. By recording from MEC cell ensembles during navigation and sleep, we found that spatial phase offsets of grid cells predict arousal-state-independent spike rate correlations. Similarly, state-invariant correlations between conjunctive grid-head-direction and pure head-direction cells were predicted by their head-direction tuning offsets. Spike rates of grid cells were only weakly correlated across modules, and module scale relationships disintegrated during slow-save sleep, suggesting that modules function as independent attractor networks. Collectively, our observations suggest that network states in MEC are expressed universally across brain and behaviour states.

neuroscience↗