Praveen K. Pilly

What a difference a parameter makes: A psychophysical comparison of random dot motion algorithms

Random dot motion (RDM) displays have emerged as one of the standard stimulus types employed in psychophysical and physiological studies of motion processing. RDMs are convenient because it is straightforward to manipulate the relative motion energy for a given motion direction in addition to stimulus parameters such as the speed, contrast, duration, density, aperture, etc. However, as widely as RDMs are employed so do they vary in their details of implementation. As a result, it is often difficult to make direct comparisons across studies employing different RDM algorithms and parameters. Here, we systematically measure the ability of human subjects to estimate motion direction for four commonly used RDM algorithms under a range of parameters in order to understand how these different algorithms compare in their perceptibility. We find that parametric and algorithmic differences can produce dramatically different performances. These effects, while surprising, can be understood in relationship to pertinent neurophysiological data regarding spatiotemporal displacement tuning properties of cells in area MT and how the tuning function changes with stimulus contrast and retinal eccentricity. These data help give a baseline by which different RDM algorithms can be compared, demonstrate a need for clearly reporting RDM details in the methods of papers, and also pose new constraints and challenges to models of motion direction processing.

How do spatial learning and memory occur in the brain? coordinated learning of entorhinal grid cells and hippocampal place cells

Spatial learning and memory are important for navigation and formation of episodic memories. The hippocampus and medial entorhinal cortex (MEC) are key brain areas for spatial learning and memory. Place cells in hippocampus fire whenever an animal is located in a specific region in the environment. Grid cells in the superficial layers of MEC provide inputs to place cells and exhibit remarkable regular hexagonal spatial firing patterns. They also exhibit a gradient of spatial scales along the dorsoventral axis of the MEC, with neighboring cells at a given dorsoventral location having different spatial phases. A neural model shows how a hierarchy of self-organizing maps, each obeying the same laws, responds to realistic rat trajectories by learning grid cells with hexagonal grid firing fields of multiple spatial scales and place cells with unimodal firing fields that fit neurophysiological data about their development in juvenile rats. The hippocampal place fields represent much larger spaces than the grid cells to support navigational behaviors. Both the entorhinal and hippocampal self-organizing maps amplify and learn to categorize the most energetic and frequent co-occurrences of their inputs. Top–down attentional mechanisms from hippocampus to MEC help to dynamically stabilize these spatial memories in both the model and neurophysiological data. Spatial learning through MEC to hippocampus occurs in parallel with temporal learning through lateral entorhinal cortex to hippocampus. These homologous spatial and temporal representations illustrate a kind of “neural relativity” that may provide a substrate for episodic learning and memory.

How entorhinal grid cells may learn multiple spatial scales from a dorsoventral gradient of cell response rates in a self-organizing map.

Place cells in the hippocampus of higher mammals are critical for spatial navigation. Recent modeling clarifies how this may be achieved by how grid cells in the medial entorhinal cortex (MEC) input to place cells. Grid cells exhibit hexagonal grid firing patterns across space in multiple spatial scales along the MEC dorsoventral axis. Signals from grid cells of multiple scales combine adaptively to activate place cells that represent much larger spaces than grid cells. But how do grid cells learn to fire at multiple positions that form a hexagonal grid, and with spatial scales that increase along the dorsoventral axis? In vitro recordings of medial entorhinal layer II stellate cells have revealed subthreshold membrane potential oscillations (MPOs) whose temporal periods, and time constants of excitatory postsynaptic potentials (EPSPs), both increase along this axis. Slower (faster) subthreshold MPOs and slower (faster) EPSPs correlate with larger (smaller) grid spacings and field widths. A self-organizing map neural model explains how the anatomical gradient of grid spatial scales can be learned by cells that respond more slowly along the gradient to their inputs from stripe cells of multiple scales, which perform linear velocity path integration. The model cells also exhibit MPO frequencies that covary with their response rates. The gradient in intrinsic rhythmicity is thus not compelling evidence for oscillatory interference as a mechanism of grid cell firing. A response rate gradient combined with input stripe cells that have normalized receptive fields can reproduce all known spatial and temporal properties of grid cells along the MEC dorsoventral axis. This spatial gradient mechanism is homologous to a gradient mechanism for temporal learning in the lateral entorhinal cortex and its hippocampal projections. Spatial and temporal representations may hereby arise from homologous mechanisms, thereby embodying a mechanistic “neural relativity” that may clarify how episodic memories are learned.

Low-level sensory plasticity during task-irrelevant perceptual learning: Evidence from conventional and double training procedures

Studies of perceptual learning have focused on aspects of learning that are related to early stages of sensory processing. However, conclusions that perceptual learning results in low-level sensory plasticity are controversial, since such learning may also be attributed to plasticity in later stages of sensory processing or in readout from sensory to decision stages, or to changes in high-level central processing. To address this controversy, we developed a novel random dot motion (RDM) stimulus to target motion cells selective to contrast polarity by ensuring the motion direction information arises only from signal dot onsets and not their offsets, and used these stimuli in the paradigm of task-irrelevant perceptual learning (TIPL). In TIPL, learning is achieved in response to a stimulus by subliminally pairing that stimulus with the targets of an unrelated training task. In this manner, we are able to probe learning for an aspect of motion processing thought to be a function of directional V1 simple cells with a learning procedure that dissociates the learned stimulus from the decision processes relevant to the training task. Our results show direction-selective learning for the designated contrast polarity that does not transfer to the opposite contrast polarity. This polarity specificity was replicated in a double training procedure in which subjects were additionally exposed to the opposite polarity. Taken together, these results suggest that TIPL for motion stimuli may occur at the stage of directional V1 simple cells. Finally, a theoretical explanation is provided to understand the data.

Spiking Neurons in a Hierarchical Self-Organizing Map Model Can Learn to Develop Spatial and Temporal Properties of Entorhinal Grid Cells and Hippocampal Place Cells

Medial entorhinal grid cells and hippocampal place cells provide neural correlates of spatial representation in the brain. A place cell typically fires whenever an animal is present in one or more spatial regions, or places, of an environment. A grid cell typically fires in multiple spatial regions that form a regular hexagonal grid structure extending throughout the environment. Different grid and place cells prefer spatially offset regions, with their firing fields increasing in size along the dorsoventral axes of the medial entorhinal cortex and hippocampus. The spacing between neighboring fields for a grid cell also increases along the dorsoventral axis. This article presents a neural model whose spiking neurons operate in a hierarchy of self-organizing maps, each obeying the same laws. This spiking GridPlaceMap model simulates how grid cells and place cells may develop. It responds to realistic rat navigational trajectories by learning grid cells with hexagonal grid firing fields of multiple spatial scales and place cells with one or more firing fields that match neurophysiological data about these cells and their development in juvenile rats. The place cells represent much larger spaces than the grid cells, which enable them to support navigational behaviors. Both self-organizing maps amplify and learn to categorize the most frequent and energetic co-occurrences of their inputs. The current results build upon a previous rate-based model of grid and place cell learning, and thus illustrate a general method for converting rate-based adaptive neural models, without the loss of any of their analog properties, into models whose cells obey spiking dynamics. New properties of the spiking GridPlaceMap model include the appearance of theta band modulation. The spiking model also opens a path for implementation in brain-emulating nanochips comprised of networks of noisy spiking neurons with multiple-level adaptive weights for controlling autonomous adaptive robots capable of spatial navigation.

Coordinated learning of grid cell and place cell spatial and temporal properties: multiple scales, attention and oscillations

A neural model proposes how entorhinal grid cells and hippocampal place cells may develop as spatial categories in a hierarchy of self-organizing maps (SOMs). The model responds to realistic rat navigational trajectories by learning both grid cells with hexagonal grid firing fields of multiple spatial scales, and place cells with one or more firing fields, that match neurophysiological data about their development in juvenile rats. Both grid and place cells can develop by detecting, learning and remembering the most frequent and energetic co-occurrences of their inputs. The models parsimonious properties include: similar ring attractor mechanisms process linear and angular path integration inputs that drive map learning; the same SOM mechanisms can learn grid cell and place cell receptive fields; and the learning of the dorsoventral organization of multiple spatial scale modules through medial entorhinal cortex to hippocampus (HC) may use mechanisms homologous to those for temporal learning through lateral entorhinal cortex to HC (‘neural relativity’). The model clarifies how top-down HC-to-entorhinal attentional mechanisms may stabilize map learning, simulates how hippocampal inactivation may disrupt grid cells, and explains data about theta, beta and gamma oscillations. The article also compares the three main types of grid cell models in the light of recent data.

How does the modular organization of entorhinal grid cells develop

The entorhinal-hippocampal system plays a crucial role in spatial cognition and navigation. Since the discovery of grid cells in layer II of medial entorhinal cortex (MEC), several types of models have been proposed to explain their development and operation; namely, continuous attractor network models, oscillatory interference models, and self-organizing map (SOM) models. Recent experiments revealing the in vivo intracellular signatures of grid cells (Domnisoru et al., 2013; Schmidt-Heiber and Hausser, 2013), the primarily inhibitory recurrent connectivity of grid cells (Couey et al., 2013; Pastoll et al., 2013), and the topographic organization of grid cells within anatomically overlapping modules of multiple spatial scales along the dorsoventral axis of MEC (Stensola et al., 2012) provide strong constraints and challenges to existing grid cell models. This article provides a computational explanation for how MEC cells can emerge through learning with grid cell properties in modular structures. Within this SOM model, grid cells with different rates of temporal integration learn modular properties with different spatial scales. Model grid cells learn in response to inputs from multiple scales of directionally-selective stripe cells (Krupic et al., 2012; Mhatre et al., 2012) that perform path integration of the linear velocities that are experienced during navigation. Slower rates of grid cell temporal integration support learned associations with stripe cells of larger scales. The explanatory and predictive capabilities of the three types of grid cell models are comparatively analyzed in light of recent data to illustrate how the SOM model overcomes problems that other types of models have not yet handled.

How reduction of theta rhythm by medial septum inactivation may covary with disruption of entorhinal grid cell responses due to reduced cholinergic transmission.

Oscillations in the coordinated firing of brain neurons have been proposed to play important roles in perception, cognition, attention, learning, navigation, and sensory-motor control. The network theta rhythm has been associated with properties of spatial navigation, as has the firing of entorhinal grid cells and hippocampal place cells. Two recent studies reduced the theta rhythm by inactivating the medial septum (MS) and demonstrated a correlated reduction in the characteristic hexagonal spatial firing patterns of grid cells. These results, along with properties of intrinsic membrane potential oscillations (MPOs) in slice preparations of medial entorhinal cortex (MEC), have been interpreted to support oscillatory interference models of grid cell firing. The current article shows that an alternative self-organizing map (SOM) model of grid cells can explain these data about intrinsic and network oscillations without invoking oscillatory interference. In particular, the adverse effects of MS inactivation on grid cells can be understood in terms of how the concomitant reduction in cholinergic inputs may increase the conductances of leak potassium (K+) and slow and medium after-hyperpolarization (sAHP and mAHP) channels. This alternative model can also explain data that are problematic for oscillatory interference models, including how knockout of the HCN1 gene in mice, which flattens the dorsoventral gradient in MPO frequency and resonance frequency, does not affect the development of the grid cell dorsoventral gradient of spatial scales, and how hexagonal grid firing fields in bats can occur even in the absence of theta band modulation. These results demonstrate how models of grid cell self-organization can provide new insights into the relationship between brain learning and oscillatory dynamics.

The neural basis of decision-making during sensemaking: Implications for human-system interaction

We have created a high-fidelity model of 9 regions of the brain involved in making sense of complex and uncertain situations. Sense making is a proactive form of situation awareness requiring sifting through information of various types to form hypotheses about evolving situations. The MINDS model (Mirroring Intelligence in a Neural Description of Sensemaking) reveals the neural principles and cognitive tradeoffs that explain weaknesses in human reasoning and decision-making.

On comparing in vivo intracranial recordings in non-human primates to predictions of optimized transcranial electrical stimulation

Transcranial electrical stimulation (tES) can be optimized to achieve maximal current flow at desired brain regions. The aim of this study was to characterize electric field magnitudes generated by tES optimization and to compare them to experimentally induced values as determined by data from intracranial electrodes. Local field potentials were recorded from two monkeys with implanted multi-site intracranial Utah arrays during transcranial direct current stimulation (tDCS), and the neural effect predictions obtained from optimized electrode placement were assessed. Comparative data between the two sites of intracranial recordings during tDCS partially validated the predictions of our tES optimization algorithms.Transcranial electrical stimulation (tES) can be optimized to achieve maximal current flow at desired brain regions. The aim of this study was to characterize electric field magnitudes generated by tES optimization and to compare them to experimentally induced values as determined by data from intracranial electrodes. Local field potentials were recorded from two monkeys with implanted multi-site intracranial Utah arrays during transcranial direct current stimulation (tDCS), and the neural effect predictions obtained from optimized electrode placement were assessed. Comparative data between the two sites of intracranial recordings during tDCS partially validated the predictions of our tES optimization algorithms.