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24 Janelia Publications

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    05/25/22 | Accurate angular integration with only a handful of neurons.
    Marcella Noorman , Brad K Hulse , Vivek Jayaraman , Sandro Romani , Ann M Hermundstad
    bioRxiv. 2022 May 25:. doi: 10.1101/2022.05.23.493052

    To flexibly navigate, many animals rely on internal spatial representations that persist when the animal is standing still in darkness, and update accurately by integrating the animal's movements in the absence of localizing sensory cues. Theories of mammalian head direction cells have proposed that these dynamics can be realized in a special class of networks that maintain a localized bump of activity via structured recurrent connectivity, and that shift this bump of activity via angular velocity input. Although there are many different variants of these so-called ring attractor networks, they all rely on large numbers of neurons to generate representations that persist in the absence of input and accurately integrate angular velocity input. Surprisingly, in the fly, Drosophila melanogaster, a head direction representation is maintained by a much smaller number of neurons whose dynamics and connectivity resemble those of a ring attractor network. These findings challenge our understanding of ring attractors and their putative implementation in neural circuits. Here, we analyzed failures of angular velocity integration that emerge in small attractor networks with only a few computational units. Motivated by the peak performance of the fly head direction system in darkness, we mathematically derived conditions under which small networks, even with as few as 4 neurons, achieve the performance of much larger networks. The resulting description reveals that by appropriately tuning the network connectivity, the network can maintain persistent representations over the continuum of head directions, and it can accurately integrate angular velocity inputs. We then analytically determined how performance degrades as the connectivity deviates from this optimally-tuned setting, and we find a trade-off between network size and the tuning precision needed to achieve persistence and accurate integration. This work shows how even small networks can accurately track an animal's movements to guide navigation, and it informs our understanding of the functional capabilities of discrete systems more broadly.

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    02/22/22 | Neural Algorithms and Circuits for Motor Planning.
    Inagaki HK, Chen S, Daie K, Finklestein A, Fontolan L, Romani S, Svoboda K
    Annual Reviews Neuroscience. 2022 Feb 22:. doi: 10.1146/annurev-neuro-092021-121730

    The brain plans and executes volitional movements. The underlying patterns of neural population activity have been explored in the context of movements of the eyes, limbs, tongue, and head in nonhuman primates and rodents. How do networks of neurons produce the slow neural dynamics that prepare specific movements and the fast dynamics that ultimately initiate these movements? Recent work exploits rapid and calibrated perturbations of neural activity to test specific dynamical systems models that are capable of producing the observed neural activity. These joint experimental and computational studies show that cortical dynamics during motor planning reflect fixed points of neural activity (attractors). Subcortical control signals reshape and move attractors over multiple timescales, causing commitment to specific actions and rapid transitions to movement execution. Experiments in rodents are beginning to reveal how these algorithms are implemented at the level of brain-wide neural circuits. Expected final online publication date for the , Volume 45 is July 2022. Please see for revised estimates.

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    12/09/21 | Bidirectional synaptic plasticity rapidly modifies hippocampal representations.
    Milstein AD, Li Y, Bittner KC, Grienberger C, Soltesz I, Magee JC, Romani S
    eLife. 2021 Dec 09;10:. doi: 10.7554/eLife.73046

    Learning requires neural adaptations thought to be mediated by activity-dependent synaptic plasticity. A relatively non-standard form of synaptic plasticity driven by dendritic calcium spikes, or plateau potentials, has been reported to underlie place field formation in rodent hippocampal CA1 neurons. Here we found that this behavioral timescale synaptic plasticity (BTSP) can also reshape existing place fields via bidirectional synaptic weight changes that depend on the temporal proximity of plateau potentials to pre-existing place fields. When evoked near an existing place field, plateau potentials induced less synaptic potentiation and more depression, suggesting BTSP might depend inversely on postsynaptic activation. However, manipulations of place cell membrane potential and computational modeling indicated that this anti-correlation actually results from a dependence on current synaptic weight such that weak inputs potentiate and strong inputs depress. A network model implementing this bidirectional synaptic learning rule suggested that BTSP enables population activity, rather than pairwise neuronal correlations, to drive neural adaptations to experience.

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    12/06/21 | Non-preferred contrast responses in the Drosophila motion pathways reveal a receptive field structure that explains a common visual illusion.
    Gruntman E, Reimers P, Romani S, Reiser MB
    Current Biology. 2021 Dec 06;31(23):5286. doi: 10.1016/j.cub.2021.09.072

    Diverse sensory systems, from audition to thermosensation, feature a separation of inputs into ON (increments) and OFF (decrements) signals. In the Drosophila visual system, separate ON and OFF pathways compute the direction of motion, yet anatomical and functional studies have identified some crosstalk between these channels. We used this well-studied circuit to ask whether the motion computation depends on ON-OFF pathway crosstalk. Using whole-cell electrophysiology, we recorded visual responses of T4 (ON) and T5 (OFF) cells, mapped their composite ON-OFF receptive fields, and found that they share a similar spatiotemporal structure. We fit a biophysical model to these receptive fields that accurately predicts directionally selective T4 and T5 responses to both ON and OFF moving stimuli. This model also provides a detailed mechanistic explanation for the directional preference inversion in response to the prominent reverse-phi illusion. Finally, we used the steering responses of tethered flying flies to validate the model's predicted effects of varying stimulus parameters on the behavioral turning inversion.

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    06/01/21 | Attractor dynamics gate cortical information flow during decision-making.
    Finkelstein A, Fontolan L, Economo MN, Li N, Romani S, Svoboda K
    Nature Neuroscience. 2021 Jun 1;24(6):843-50. doi: 10.1038/s41593-021-00840-6

    Decisions are held in memory until enacted, which makes them potentially vulnerable to distracting sensory input. Gating of information flow from sensory to motor areas could protect memory from interference during decision-making, but the underlying network mechanisms are not understood. Here, we trained mice to detect optogenetic stimulation of the somatosensory cortex, with a delay separating sensation and action. During the delay, distracting stimuli lost influence on behavior over time, even though distractor-evoked neural activity percolated through the cortex without attenuation. Instead, choice-encoding activity in the motor cortex became progressively less sensitive to the impact of distractors. Reverse engineering of neural networks trained to reproduce motor cortex activity revealed that the reduction in sensitivity to distractors was caused by a growing separation in the neural activity space between attractors that encode alternative decisions. Our results show that communication between brain regions can be gated via attractor dynamics, which control the degree of commitment to an action.

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    03/01/21 | Mapping Low-Dimensional Dynamics to High-Dimensional Neural Activity: A Derivation of the Ring Model from the Neural Engineering Framework.
    Barak O, Romani S
    Neural Computation. 2021 Mar 01;33(3):827-52. doi: 10.1162/neco_a_01361

    Empirical estimates of the dimensionality of neural population activity are often much lower than the population size. Similar phenomena are also observed in trained and designed neural network models. These experimental and computational results suggest that mapping low-dimensional dynamics to high-dimensional neural space is a common feature of cortical computation. Despite the ubiquity of this observation, the constraints arising from such mapping are poorly understood. Here we consider a specific example of mapping low-dimensional dynamics to high-dimensional neural activity-the neural engineering framework. We analytically solve the framework for the classic ring model-a neural network encoding a static or dynamic angular variable. Our results provide a complete characterization of the success and failure modes for this model. Based on similarities between this and other frameworks, we speculate that these results could apply to more general scenarios.

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    10/29/20 | The Statistical Structure of the Hippocampal Code for Space as a Function of Time, Context, and Value.
    Lee JS, Briguglio JJ, Cohen JD, Romani S, Lee AK
    Cell. 2020 Oct 29;183(3):620-35. doi: 10.1016/j.cell.2020.09.024

    Hippocampal activity represents many behaviorally important variables, including context, an animal's location within a given environmental context, time, and reward. Using longitudinal calcium imaging in mice, multiple large virtual environments, and differing reward contingencies, we derived a unified probabilistic model of CA1 representations centered on a single feature-the field propensity. Each cell's propensity governs how many place fields it has per unit space, predicts its reward-related activity, and is preserved across distinct environments and over months. Propensity is broadly distributed-with many low, and some very high, propensity cells-and thus strongly shapes hippocampal representations. This results in a range of spatial codes, from sparse to dense. Propensity varied ∼10-fold between adjacent cells in salt-and-pepper fashion, indicating substantial functional differences within a presumed cell type. Intracellular recordings linked propensity to cell excitability. The stability of each cell's propensity across conditions suggests this fundamental property has anatomical, transcriptional, and/or developmental origins.

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    01/10/20 | Fundamental law of memory recall.
    Naim M, Katkov M, Romani S, Tsodyks M
    Physical Review Letters. 2020 Jan 10;124(1):018101. doi: 10.1103/PhysRevLett.124.018101

    Human memory appears to be fragile and unpredictable. Free recall of random lists of words is a standard paradigm used to probe episodic memory. We proposed an associative search process that can be reduced to a deterministic walk on random graphs defined by the structure of memory representations. The corresponding graph model can be solved analytically, resulting in a novel parameter-free prediction for the average number of memory items recalled (R) out of M items in memory: R=sqrt[3πM/2]. This prediction was verified with a specially designed experimental protocol combining large-scale crowd-sourced free recall and recognition experiments with randomly assembled lists of words or common facts. Our results show that human memory can be described by universal laws derived from first principles.

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    12/11/19 | The computation of directional selectivity in the OFF motion pathway.
    Gruntman E, Romani S, Reiser MB
    eLife. 2019 Dec 11;8:. doi: 10.7554/eLife.50706

    In flies, the direction of moving ON and OFF features is computed separately. T4 (ON) and T5 (OFF) are the first neurons in their respective pathways to extract a directionally selective response from their non-selective inputs. Our recent study of T4 found that the integration of offset depolarizing and hyperpolarizing inputs is critical for the generation of directional selectivity. However, T5s lack small-field inhibitory inputs, suggesting they may use a different mechanism. Here we used whole-cell recordings of T5 neurons and found a similar receptive field structure: fast depolarization and persistent, spatially offset hyperpolarization. By assaying pairwise interactions of local stimulation across the receptive field, we found no amplifying responses, only suppressive responses to the non-preferred motion direction. We then evaluated passive, biophysical models and found that a model using direct inhibition, but not the removal of excitation, can accurately predict T5 responses to a range of moving stimuli.

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    11/20/19 | Generation of stable heading representations in diverse visual scenes.
    Kim SS, Hermundstad AM, Romani S, Abbott LF, Jayaraman V
    Nature. 2019 Nov 20;576(7785):126-31. doi: 10.1038/s41586-019-1767-1

    Many animals rely on an internal heading representation when navigating in varied environments. How this representation is linked to the sensory cues that define different surroundings is unclear. In the fly brain, heading is represented by 'compass' neurons that innervate a ring-shaped structure known as the ellipsoid body. Each compass neuron receives inputs from 'ring' neurons that are selective for particular visual features; this combination provides an ideal substrate for the extraction of directional information from a visual scene. Here we combine two-photon calcium imaging and optogenetics in tethered flying flies with circuit modelling, and show how the correlated activity of compass and visual neurons drives plasticity, which flexibly transforms two-dimensional visual cues into a stable heading representation. We also describe how this plasticity enables the fly to convert a partial heading representation, established from orienting within part of a novel setting, into a complete heading representation. Our results provide mechanistic insight into the memory-related computations that are essential for flexible navigation in varied surroundings.

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