During navigation, grid cells increase their spike rates in firing fields arranged on a strikingly regular triangular lattice, while their spike timing is often modulated by theta oscillations. Oscillatory interference models of grid cells predict theta amplitude modulations of membrane potential during firing field traversals, while competing attractor network models predict slow depolarizing ramps. Here, using in-vivo whole-cell recordings, we tested these models by directly measuring grid cell intracellular potentials in mice running along linear tracks in virtual reality. Grid cells had large and reproducible ramps of membrane potential depolarization that were the characteristic signature tightly correlated with firing fields. Grid cells also exhibited intracellular theta oscillations that influenced their spike timing. However, the properties of theta amplitude modulations were not consistent with the view that they determine firing field locations. Our results support cellular and network mechanisms in which grid fields are produced by slow ramps, as in attractor models, while theta oscillations control spike timing.
The vertebrate hindbrain contains various sensory-motor networks controlling movements of the eyes, jaw, head, and body. Here we show that stripes of neurons with shared neurotransmitter phenotype that extend throughout the hindbrain of young zebrafish reflect a broad underlying structural and functional patterning. The neurotransmitter stripes contain cell types with shared gross morphologies and transcription factor markers. Neurons within a stripe are stacked systematically by extent and location of axonal projections, input resistance, and age, and are recruited along the axis of the stripe during behavior. The implication of this pattern is that the many networks in hindbrain are constructed from a series of neuronal components organized into stripes that are ordered from top to bottom according to a neuron's age, structural and functional properties, and behavioral roles. This simple organization probably forms a foundation for the construction of the networks underlying the many behaviors produced by the hindbrain.interneuron | locomotion | recruitment | topography T he hindbrain contains a diverse set of sensory-motor networks that control movements required for vision, respiration, mastication, and locomotion in all vertebrates (1, 2). Most often these different networks are studied separately from one another, perhaps because the behaviors are distinct, and the regional differentiation of hindbrain suggests that its several networks might have little in common. Thus, we have strong data for the hindbrain control of eye movements, respiration, and locomotion (3-10), but fewer unifying principles of structural and functional organization that apply across the different networks.Structurally, the hindbrain is divided into segments, called rhombomeres, which differ in the expression of homeotic genes, in the morphological differentiation of neurons, and in their sensory inputs and motor outputs (2, 11). Though there are clear distinctions among rhombomeres, there are indications from previous developmental work using in situ staining for transcription factors and backfilling of hindbrain neurons that there may be structural patterns that cross rhombomere boundaries (12-16). Prior work has also revealed parallels in the development of hindbrain and spinal cord, with the hindbrain sharing features of the now-classic transcription factor code that directs development in spinal cord (17)(18)(19)(20)(21)(22). Though these studies did not explore function because they were performed during early development, they raised the possibility of a broader structuralfunctional patterning that spans rhomobomeres and may underlie the organization of circuits for different behaviors.Here we show that there is indeed a broad structural and functional patterning of neurons in the hindbrain of young zebrafish. The work was initially prompted by a striking patterning observed in earlier work in which we used in situ staining for markers of neurotransmitter phenotype to reveal putative glycinergic, GABAergic, and glutamatergic ...
Summary: How the topography of neural circuits relates to their function remains unclear. Although topographic maps exist for sensory and motor variables, they are rarely observed for cognitive variables. Using calcium imaging during virtual navigation, we investigated the relationship between the anatomical organization and functional properties of grid cells, which represent a cognitive code for location during navigation. We found a substantial degree of grid cell micro-organization in mouse medial entorhinal cortex: grid cells and modules all clustered anatomically. Within a module, the layout of grid cells was a noisy two-dimensional lattice, in which the anatomical distribution of grid cells largely matched their spatial tuning phases. This micro-arrangement of phases demonstrates the existence of a topographical map encoding a cognitive variable in rodents. It contributes to a foundation for evaluating circuit models of the grid cell network, and is consistent with continuous attractor models as the mechanism of grid formation.
The hindbrain of larval zebrafish contains a relatively simple ground plan in which the neurons throughout it are arranged into stripes that represent broad neuronal classes that differ in transmitter identity, morphology, and transcription factor expression. Within the stripes, neurons are stacked continuously according to age as well as structural and functional properties, such as axonal extent, input resistance, and the speed at which they are recruited during movements. Here we address the question of how particular networks among the many different sensory-motor networks in hindbrain arise from such an orderly plan. We use a combination of transgenic lines and pairwise patch recording to identify excitatory and inhibitory interneurons in the hindbrain network for escape behaviors initiated by the Mauthner cell. We map this network onto the ground plan to show that an individual hindbrain network is built by drawing components in predictable ways from the underlying broad patterning of cell types stacked within stripes according to their age and structural and functional properties. Many different specialized hindbrain networks may arise similarly from a simple early patterning.T he vertebrate hindbrain contains many different sensorymotor networks that control movements of structures in the body and the head. Our recent work shows that despite the diverse networks it contains, there is a remarkably orderly patterning of neurons that extends throughout the hindbrain in young zebrafish, across the well-studied segments, or rhombomeres (1-4). This pattern consists of a series of neurotransmitter stripes that represent broad neuronal classes that differ in transmitter identity, morphology, and transcription factor expression. Within these stripes, neurons are stacked continuously according to age as well as structural and functional characteristics, such as axonal extent, input resistance, and the speed at which they are recruited during movements.The presence of such an orderly array of neurons suggests that networks are built by drawing components from particular stripes that contain cell types with the required structure and transmitter phenotype, and from the particular position within a stripe occupied by neurons with the appropriate functional properties, much like selecting parts from a catalog. Here we test this possibility through a study of the hindbrain network for the escape behavior initiated by the Mauthner cell (M-cell) (5-8). We conclusively identify neurons in the hindbrain escape network of the M-cell in zebrafish and map each cell type onto the arrangement into the stripes that we describe in the previous work. Our work reveals that this network is built from neurons in predictable locations that are consistent with the idea that the stripe patterning in hindbrain represents an orderly array of neurons from which network components are drawn. Many different hindbrain networks probably arise in a similar way by drawing neurons from a shared structurally and functionally ordered set of parts. ...
SUMMARY Grid cells, defined by their striking periodic spatial responses in open 2D arenas, appear to respond differently on 1D tracks: the multiple response fields are not periodically arranged, peak amplitudes vary across fields, and the mean spacing between fields is larger than in 2D environments. We ask whether such 1D responses are consistent with the system’s 2D dynamics. Combining analytical and numerical methods, we show that the 1D responses of grid cells with stable 1D fields are consistent with a linear slice through a 2D triangular lattice. Further, the 1D responses of comodular cells are well described by parallel slices, and the offsets in the starting points of the 1D slices can predict the measured 2D relative spatial phase between the cells. From these results, we conclude that the 2D dynamics of these cells is preserved in 1D, suggesting a common computation during both types of navigation behavior.
During spatial navigation, animals use self-motion to estimate positions through path integration. However, estimation errors accumulate over time and it is unclear how they are corrected. Here we report a new cell class (‘cue cell’) encoding visual cues that could be used to correct errors in path integration in mouse medial entorhinal cortex (MEC). During virtual navigation, individual cue cells exhibited firing fields only near visual cues and their population response formed sequences repeated at each cue. These cells consistently responded to cues across multiple environments. On a track with cues on left and right sides, most cue cells only responded to cues on one side. During navigation in a real arena, they showed spatially stable activity and accounted for 32% of unidentified, spatially stable MEC cells. These cue cell properties demonstrate that the MEC contains a code representing spatial landmarks, which could be important for error correction during path integration.
Objective. Recovery of voluntary gait after spinal cord injury (SCI) requires the restoration of effective motor cortical commands, either by means of a mechanical connection to the limbs, or by restored functional connections to muscles. The latter approach might use functional electrical stimulation (FES), driven by cortical activity, to restore voluntary movements. Moreover, there is evidence that this peripheral stimulation, synchronized with patients' voluntary effort, can strengthen descending projections and recovery. As a step towards establishing such a cortically-controlled FES system for restoring function after SCI, we evaluate here the type and quantity of neural information needed to drive such a brain machine interface (BMI) in rats. We compared the accuracy of the predictions of hindlimb electromyograms (EMG) and kinematics using neural data from an intracortical array and a less-invasive epidural array. Approach. Seven rats were trained to walk on a treadmill with a stable pattern. One group of rats (n = 4) was implanted with intracortical arrays spanning the hindlimb sensorimotor cortex and EMG electrodes in the contralateral hindlimb. Another group (n = 3) was implanted with epidural arrays implanted on the dura overlying hindlimb sensorimotor cortex. EMG, kinematics and neural data were simultaneously recorded during locomotion. EMGs and kinematics were decoded using linear and nonlinear methods from multiunit activity and field potentials. Main results. Predictions of both kinematics and EMGs were effective when using either multiunit spiking or local field potentials (LFPs) recorded from intracortical arrays. Surprisingly, the signals from epidural arrays were essentially uninformative. Results from somatosensory evoked potentials (SSEPs) confirmed that these arrays recorded neural activity, corroborating our finding that this type of array is unlikely to
17During spatial navigation, animals use self-motion to estimate positions through path integration. 18However, estimation errors accumulate over time and it is unclear how they are corrected. Here we report 19 a new cell class ("cue cell") in mouse medial entorhinal cortex (MEC) that encoded visual cue 20information that could be used to correct errors in path integration. Cue cells accounted for a large 21 fraction of unidentified MEC cells. They exhibited firing fields only near visual cues during virtual 22 navigation and spatially stable activity during navigation in a real arena. Cue cells' responses occurred in 23 sequences repeated at each cue and were likely driven by visual inputs. In layers 2/3 of the MEC, cue 24 cells formed clusters. Anatomically adjacent cue cells responded similarly to cues. These cue cell 25properties demonstrate that the MEC circuits contain a code representing spatial landmarks that could 26 play a significant role in error correction during path integration. 28Animals navigate using landmarks, objects or features that provide sensory cues, to estimate spatial 29 location. When sensory cues defining position are either absent or unreliable during navigation, many 30 animals can use self-motion to update internal representations of location through path integration 31 (Mittelstaedt, 1982;Tsoar et al., 2011). A set of interacting brain regions, including the entorhinal cortex, 32parietal cortex, and the hippocampus (Brun et al.,
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