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Jayakumar, R. P.

Publications and source records attributed to Jayakumar, R. P..

6 recordsLinked to original sources

Hippocampal theta frequency as a readout of path-integration recalibration

Understanding how the brain represents hidden variables is a fundamental challenge. In navigation, the internal path-integration gain is often masked by external landmarks that override the path integrator. Path integration can recalibrate its gain when allothetic and idiothetic cues conflict, but the real-time dynamics of this process are hidden to direct observation. Here, we demonstrate that theta frequency provides an error signal between the observable hippocampal gain and the internal path-integration gain. Theta frequency decreased as conflict between landmark-driven hippocampal gain and path-integration gain increased and recovered as the path-integration gain recalibrated to the new gain. A continuous attractor model replicated these dynamics, suggesting that the theta-frequency drop is driven by the misalignment of allothetic and idiothetic inputs, reducing the excitatory drive to the network. Thus, theta frequency provides a real-time readout of internal gain-error signals, offering a novel methodology to estimate hidden cognitive variables through observable physiological oscillations.

neuroscience↗

Synchronized path-integration recalibration but distinct landmark-control dynamics in head direction and CA1 place cells

Accurate spatial navigation relies on path integration, a process of tracking ones location by integrating self-motion cues. Path integration uses a gain factor relating self-motion signals to displacement on the cognitive map. This gain is plastic, recalibrating rapidly to match perceived displacements relative to external cues. To elucidate the mechanism of recalibration, we simultaneously recorded from place cells, which instantiate the cognitive map, and head direction (HD) cells, thought to orient the map. Persistent conflict between self-motion and visual feedback induced functionally identical recalibration of path-integration gain in the two neural populations during forward locomotion; however, during locomotor immobility accompanied by head-scanning, HD cells did not exhibit recalibration. Moreover, the two populations manifested differential field-shifting dynamics relative to landmarks during recalibration. These results uncover a tightly coordinated yet behavior-dependent recalibration process across the navigation circuit that achieves a robust yet flexible coupling of the internal sense of position and direction.

neuroscience↗

Closed-loop control and recalibration of place cells by optic flow

Understanding the interplay between sensory input, endogenous neural dynamics, and behavioral output is key toward understanding the principles of neural computation. Hippocampal place cells are an ideal system to investigate this closed-loop interaction, as they are influenced by both self-motion (idiothetic) signals and by external sensory landmarks as an animal navigates its environment1-9. To continuously update a position signal on an internal "cognitive map", the hippocampal system integrates self-motion signals over time10,11. In the absence of stable, external landmarks, however, these spatial correlates of neuronal activity can quickly accumulate error and cause the internal representation of position or direction to drift relative to the external environment1,5. We have previously demonstrated that, in addition to their known roles in preventing and/or correcting path-integration error, external landmarks can be used as a putative teaching signal to recalibrate the gain of the path integration system6. However, it remains unclear whether idiothetic cues, such as optic flow, exert sufficient influence on the cognitive map to enable recalibration of path integration, or if instead an unambiguous allocentric frame of reference, anchored by polarizing landmark information, is essential for path integration recalibration. Here, we use principles of control theory12,13 to demonstrate systematic control of place fields by pure optic flow information in freely moving animals by using a neurally closed-loop virtual reality system that adjusts optic flow speed as a function of real-time decoding of the hippocampal spatial map. Using this "cognitive clamp", we show that we can not only bring the updating of the map under control of the optic flow cues but we can also elicit recalibration of path integration. This finding demonstrates that the brain continuously rebalances the influence of conflicting idiothetic cues to fine-tune the neural dynamics of path integration, and that this recalibration process does not require a top-down, unambiguous position signal from landmarks.

neuroscience↗

Advances in non-invasive tracking of wave-type electric fish in natural and laboratory settings

Recent technological advances greatly improved the possibility to study freely behaving animals in natural conditions. However, many systems still rely on animal-mounted devices, which can already bias behavioral observations. Alternatively, animal behaviors can be detected and tracked in recordings of stationary sensors, e.g. video cameras. While these approaches circumvent the influence of animal-mounted devices, identification of individuals is much more challenging. We take advantage of the individual-specific electric fields electric fish generate by discharging their electric organ (EOD) to record and track their movement and communication behaviors without interfering with the animals themselves. EODs of complete groups of fish can be recorded with electrode arrays submerged in the water and then be tracked for individual fish. Here, we present an improved algorithm for tracking electric signals of wave-type electric fish with unprecedented accuracy. Our algorithm benefits from combining and refining previous approaches of tracking individual specific EOD frequencies (EODf) and spatial electric field properties. In this process, the similarity of signal pairs in extended data windows determines their tracking order, making the algorithm more robust against detection losses and intersections. We quantify the performance of the algorithm and show its application for a data set recorded with a 64-electrode array in a stream in the Llanos, Colombia, where we managed, for the first time, to track Apteronotus leptorhynchus over many days. These technological advances make electric fish a unique model system for a detailed analysis of social and communication behaviors, with strong implications for our research on sensory coding.

animal behavior and cognition↗

Wide-Angle, Monocular Head Tracking using Passive Markers

Camera images can encode large amounts of visual information of an animal and its environment, enabling high fidelity 3D reconstruction of the animal and its environment using computer vision methods. Most systems, both markerless (e.g. deep learning based) and marker-based, require multiple cameras to track features across multiple points of view to enable such 3D reconstruction. However, such systems can be expensive and are challenging to set up in small animal research apparatuses. We present an open-source, marker-based system for tracking the head of a rodent for behavioral research that requires only a single camera with a potentially wide field of view. The system features a lightweight visual target and computer vision algorithms that together enable high-accuracy tracking of the six-degree-of-freedom position and orientation of the animals head. The system, which only requires a single camera positioned above the behavioral arena, robustly reconstructs the pose over a wide range of head angles (360{whitebullet} in yaw, and approximately {+/-}120{whitebullet} in roll and pitch). Experiments with live animals demonstrate that the system can reliably identify rat head position and orientation. Evaluations using a commercial optical tracker device show that the system achieves accuracy that rivals commercial multi-camera systems. Our solution significantly improves upon existing monocular marker-based tracking methods, both in accuracy and in allowable range of motion. The proposed system enables the study of complex behaviors by providing robust, fine-scale measurements of rodent head motions in a wide range of orientations.

neuroscience↗

Recalibration of path integration in hippocampal place cells

Hippocampal place cells are spatially tuned neurons that serve as elements of a \"cognitive map\" in the mammalian brain1. To detect the animals location, place cells are thought to rely upon two interacting mechanisms: sensing the animals position relative to familiar landmarks2,3 and measuring the distance and direction that the animal has travelled from previously occupied locations4-7. The latter mechanism, known as path integration, requires a finely tuned gain factor that relates the animals self-movement to the updating of position on the internal cognitive map, with external landmarks necessary to correct positional error that eventually accumulates8,9. Path-integration-based models of hippocampal place cells and entorhinal grid cells treat the path integration gain as a constant9-14, but behavioral evidence in humans suggests that the gain is modifiable15. Here we show physiological evidence from hippocampal place cells that the path integration gain is indeed a highly plastic variable that can be altered by persistent conflict between self-motion cues and feedback from external landmarks. In a novel, augmented reality system, visual landmarks were moved in proportion to the animals movement on a circular track, creating continuous conflict with path integration. Sustained exposure to this cue conflict resulted in predictable and prolonged recalibration of the path integration gain, as estimated from the place cells after the landmarks were extinguished. We propose that this rapid plasticity keeps the positional update in register with the animals movement in the external world over behavioral timescales (mean 50 laps over 35 minutes). These results also demonstrate that visual landmarks not only provide a signal to correct cumulative error in the path integration system, as has been previously shown4,8,16-19, but also rapidly fine-tune the integration computation itself.

neuroscience↗