Functional dissection of circuitry in a neural integrator

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

doi:10.1038/nn1877

Cited by 135Neural dynamics and brain functionMemory and Neural MechanismsMotor Control and Adaptation

Functional dissection of circuitry in a neural integrator

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Aksay, Emre, Olasagasti, Itsaso, Mensh, Brett D, Baker, Robert, Goldman, Mark S, Tank, David W·2007·Nature Neuroscience

DOI 10.1038/nn1877PMC PMC2803116

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Abstract

In neural integrators, transient inputs are accumulated into persistent firing rates that are a neural correlate of short-term memory. Integrators often contain two opposing cell populations that increase and decrease sustained firing as a stored parameter value rises. A leading hypothesis for the mechanism of persistence is positive feedback through mutual inhibition between these opposing populations. We tested predictions of this hypothesis in the goldfish oculomotor velocity-to-position integrator by measuring the eye position and firing rates of one population, while pharmacologically silencing the opposing one. In complementary experiments, we measured responses in a partially silenced single population. Contrary to predictions, induced drifts in neural firing were limited to half of the oculomotor range. We built network models with synaptic-input thresholds to demonstrate a new hypothesis suggested by these data: mutual inhibition between the populations does not provide positive feedback in support of integration, but rather coordinates persistent activity intrinsic to each population.

Integrity signals

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Crossref · 10.1038/nn1877

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Within the oculomotor integrator, broad physiological and coarse anatomical evidence implicates recurrent excitatory interactions in generating attractor dynamics.
“Within the oculomotor integrator, there is broad physiological18–20 and coarse anatomical21 evidence implicating recurrent excitatory interactions in generating attractor dynamics.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [20]
Persistent activity in the oculomotor integrator is generated independently by each half of the brain.
“physiological studies indicating that persistent activity in the oculomotor integrator is generated independently by each half of the brain20,43,44.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [20]
Previous experiments have shown that one-half of the VPNI is capable of maintaining the ipsilateral range of eye positions after the contralateral half of the VPNI is silenced.
“Although the VPNI is a bilateral circuit, previous experiments20,56 have shown that one-half of the VPNI is nevertheless capable of maintaining the ipsilateral range of eye positions after the contralateral half of the VPNI is silenced.”
From Predicting modular functions and neural coding of behavior from a synaptic wiring diagram (2024) · cites this paper as [20]

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History Dependence of Rate Covariation between Neurons during Persistent Activity
Integrator, I. A. O. (2008)

Authors: Aksay, E., Olasagasti, I., Mensh, B. D., Baker, R., Goldman, M. S., & Tank, D. W.
Affiliations: Cornell University (US)
Wellesley College (US)
Harvard University (US)
NYU Langone Health (US)
Princeton University (US)
Corresponding author: Aksay, Emre
Goldman, Mark S
ORCID: Aksay, Emre
Olasagasti, Itsaso
Mensh, Brett D
Baker, Robert
Goldman, Mark S
Tank, David W
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2007-03-18
Volume: 10
Issue: 4
Pages: 494-504
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/nn1877
PMC: PMC2803116
OpenAlex: W2102972654
Cited by: 134
References: 49
Citations by year: 2026: 6 · 2025: 7 · 2024: 10 · 2023: 2 · 2022: 7 · 2021: 9 · 2020: 6 · 2019: 7 · 2018: 6 · 2017: 9 · 2016: 7 · 2015: 8 · 2014: 7 · 2013: 8 · 2012: 6
FWCI: 3.34
Type: journal article
Language: en
Update notices: erratum (2007-06-01)
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (R01MH069726)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
Keywords: neural integrator, short-term memory, persistent activity, reciprocal inhibition, positive feedback, eye position, network models, neural circuits
MeSH terms: Action Potentials, Anesthetics, Local, Animals, Behavior, Animal, Brain, Computer Simulation, Eye Movements, Feedback, Goldfish, Lidocaine, Models, Neurological, Nerve Block, Nerve Net, Neurons, Ocular Physiological Phenomena, Dominance, Ocular

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Functional dissection of circuitry in a neural integrator

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