Functional dissection of circuitry in a neural integrator

Aksay, Emre; Olasagasti, Itsaso; Mensh, Brett D.; Baker, R.; Goldman, Mark S.; Tank, David W.

doi:10.1038/nn1877

Cited by 117 publications

(178 citation statements)

References 50 publications

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“…Crawford and Vilis (1993) provided evidence for multiple vertical/torsional integrators when they pharmacologically inhibited the integrator and found that the eye did not drift to a single resting position, but rather, multiple resting positions were possible. Recent experimental findings in goldfish also support the hypothesis of separate integrators for horizontal gaze (Aksay et al 2007). …”

Section: Multiple Horizontal Nismentioning

confidence: 65%

Alexander’s Law in Patients with Acute Vestibular Tone Asymmetry—Evidence for Multiple Horizontal Neural Integrators

Hegemann

Straumann

Bockisch

2007

JARO

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Alexander_s law (AL) states that the slow-phase velocity of spontaneous nystagmus of peripheral vestibular origin is dependent on horizontal gaze position, with greater velocity when gaze is directed in the fast-phase direction. AL is thought to be a compensatory reaction resulting from adaptive changes in the horizontal ocular motor neural integrator. Until now, only horizontal eye movements have been investigated with respect to AL. Because spontaneous nystagmus usually includes vertical and torsional components, we asked whether horizontal gaze changes would have an effect on the 3D drift of spontaneous nystagmus and, thus, on the vertical/ torsional neural integrator. We hypothesized that AL reduces all nystagmus components proportionally. Moreover, we questioned the classical theory of a single bilaterally organized horizontal integrator and searched for nonlinearities of AL implying a network of multiple integrators. Using dual scleral search coils, we measured AL in 17 patients with spontaneous nystagmus. Patients followed a pulsed laser dot at eye level jumping in 5-steps along the horizontal meridian between 25-right and left in otherwise complete darkness. AL was observed in 15 of 17 patients. Whereas individual patients typically showed a change of 3D-drift direction at different horizontal eye positions, the average change in direction was not different from zero. The strength of AL (= rate of change of total velocity with gaze position) correlated with nystagmus slow-phase velocity (Spearman_s rho=0.5; pG0.05) and, on average, did not change the 3D nystagmus drift direction. In general, eye velocity did not vary linearly with eye position. Rather, there was a stronger dependence of velocity on horizontal position when subjects looked in the slow-phase direction compared to the fast-phase direction. We conclude that the theory of a simple leak of a single horizontal neural integrator is not sufficient to explain all aspects of AL.

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Section: Multiple Horizontal Nismentioning

confidence: 65%

Alexander’s Law in Patients with Acute Vestibular Tone Asymmetry—Evidence for Multiple Horizontal Neural Integrators

Hegemann

Straumann

Bockisch

2007

JARO

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“…The small effect seen on activity with contralateral inhibition (Extended Data Figs 2e, 8d) implies further that ALM hemispheres function as "modules", maintaining preparatory activity independently 28 . After unilateral perturbation, information from the unperturbed side helps recover function of the perturbed side.…”

Section: Contralateral Input Is Required For Recoverymentioning

confidence: 94%

Robust neuronal dynamics in premotor cortex during motor planning

Li¹,

Daie²,

Svoboda³

et al. 2016

Nature

421

485

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Neural activity maintains representations that bridge past and future events, often over many seconds. Network models can produce persistent and ramping activity, but the positive feedback that is critical for these slow dynamics can cause sensitivity to perturbations. Here we use electrophysiology and optogenetic perturbations in mouse premotor cortex to probe robustness of persistent neural representations during motor planning. Preparatory activity is remarkably robust to large-scale unilateral silencing: detailed neural dynamics that drive specific future movements were quickly and selectively restored by the network. Selectivity did not recover after bilateral silencing of premotor cortex. Perturbations to one hemisphere are thus corrected by information from the other hemisphere. Corpus callosum bisections demonstrated that premotor cortex hemispheres can maintain preparatory activity independently. Redundancy across selectively coupled modules, as we observed in premotor cortex, is a hallmark of robust control systems. Network models incorporating these principles show robustness that is consistent with data.

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“…Despite extensive efforts to identify biological persistent activity modes mediated by recurrent excitatory synaptic connections 48 , very little experimental evidence supports the classic hypothesis that reverberant network activity functions to encode and maintain information proposed by Hebb 9 . Our finding that sequential stimulation did not reset hilar persistent activity to a new state corresponding to the most recent stimulus is also inconsistent with the predictions from theoretical studies employing attractor-based networks with recurrent connectivity 49 .…”

Section: Relationship To Delay-period Activity Recorded During Workinmentioning

confidence: 99%

Mnemonic representations of transient stimuli and temporal sequences in the rodent hippocampus in vitro

Hyde

Strowbridge

2012

Nat Neurosci

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A primary function of the brain is to store and retrieve information. Except for working memory, where extracellular recordings demonstrate persistent discharges during delay-response tasks, it has been difficult to link memories with changes in individual neurons or specific synaptic connections. Here, we demonstrate that transient stimuli are reliably encoded in the ongoing activity of brain tissue in vitro. We found that the patterns of synaptic input onto dentate hilar neurons predict which of four pathways were stimulated with an accuracy of 76% and performed significantly better than chance for >15 s. Dentate gyrus neurons also could accurately encode temporal sequences using population representations that were robust to variation in sequence interval. These results demonstrate direct neural encoding of temporal sequences in the spontaneous activity of brain tissue and suggest a novel local circuit mechanism that may contribute to diverse forms of short-term memory.A fundamental property of the central nervous system is the ability to encode and retrieve information. In mammals, declarative memory function is typically divided into behavioral tasks that promote short-or long-term storage of items such as names, places and specific temporal sequences 1,2 . While the specific cellular origin of individual long-term declarative memories has remained elusive, a large literature highlights the importance of several critical brain regions, including the prefrontal cortex 3 and the hippocampal formation 4 for encoding short-term, or working, memories. Extracellular unit recordings in these brain areas often display periods of persistent spiking activity at elevated frequencies when animals are required to retain transiently presented sensory information. This "delay-period activity" typically lasts for seconds and is extinguished when the animal initiates a behavioral response to indicate whether it correctly remembered the correct transient stimulus 3,5 . The reduction in persistent spiking during error trials-trials in which the animal made an incorrect behavioral response following the delay period-argues that delay-period activity in those specific neurons reflects activity in neural circuits encoding that short-term memory, rather than a response to the cue stimulus or a motor plan Users may view, print, copy, download and text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use:

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Functional dissection of circuitry in a neural integrator

Cited by 117 publications

References 50 publications

Alexander’s Law in Patients with Acute Vestibular Tone Asymmetry—Evidence for Multiple Horizontal Neural Integrators

Alexander’s Law in Patients with Acute Vestibular Tone Asymmetry—Evidence for Multiple Horizontal Neural Integrators

Robust neuronal dynamics in premotor cortex during motor planning

Mnemonic representations of transient stimuli and temporal sequences in the rodent hippocampus in vitro

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