Effects of muscarinic and nicotinic receptors on contextual modulation in macaque
      area V1

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Abstract

Context affects the salience and visibility of image elements in visual scenes. Collinear flankers can enhance or decrease the perceptual and neuronal sensitivity to flanked stimuli. These effects are mediated through lateral interactions between neurons in the primary visual cortex (area V1), in conjunction with feedback from higher visual areas. The strength of lateral interactions is affected by cholinergic neuromodulation. Blockade of muscarinic receptors should increase the strength of lateral intracortical interactions, while nicotinic blockade should reduce thalamocortical feed-forward drive. Here we test this proposal through local iontophoretic application of the muscarinic receptor antagonist scopolamine and the nicotinic receptor antagonist mecamylamine, while recording single cells in parafoveal representations in awake fixating macaque V1. Collinear flankers generally reduced neuronal contrast sensitivity. Muscarinic and nicotinic receptor blockade equally reduced neuronal contrast sensitivity. Contrary to our hypothesis, flanker interactions were not systematically affected by either receptor blockade.

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Uncertainty, neuromodulation, and attention.

Angela Yu, Peter Dayan (2005)

Uncertainty in various forms plagues our interactions with the environment. In a Bayesian statistical framework, optimal inference and prediction, based on unreliable observations in changing contexts, require the representation and manipulation of different forms of uncertainty. We propose that the neuromodulators acetylcholine and norepinephrine play a major role in the brain's implementation of these uncertainty computations. Acetylcholine signals expected uncertainty, coming from known unreliability of predictive cues within a context. Norepinephrine signals unexpected uncertainty, as when unsignaled context switches produce strongly unexpected observations. These uncertainty signals interact to enable optimal inference and learning in noisy and changeable environments. This formulation is consistent with a wealth of physiological, pharmacological, and behavioral data implicating acetylcholine and norepinephrine in specific aspects of a range of cognitive processes. Moreover, the model suggests a class of attentional cueing tasks that involve both neuromodulators and shows how their interactions may be part-antagonistic, part-synergistic.

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Modes and models of forebrain cholinergic neuromodulation of cognition.

Michael E. Hasselmo, Martin Sarter (2011)

As indicated by the profound cognitive impairments caused by cholinergic receptor antagonists, cholinergic neurotransmission has a vital role in cognitive function, specifically attention and memory encoding. Abnormally regulated cholinergic neurotransmission has been hypothesized to contribute to the cognitive symptoms of neuropsychiatric disorders. Loss of cholinergic neurons enhances the severity of the symptoms of dementia. Cholinergic receptor agonists and acetylcholinesterase inhibitors have been investigated for the treatment of cognitive dysfunction. Evidence from experiments using new techniques for measuring rapid changes in cholinergic neurotransmission provides a novel perspective on the cholinergic regulation of cognitive processes. This evidence indicates that changes in cholinergic modulation on a timescale of seconds is triggered by sensory input cues and serves to facilitate cue detection and attentional performance. Furthermore, the evidence indicates cholinergic induction of evoked intrinsic, persistent spiking mechanisms for active maintenance of sensory input, and planned responses. Models have been developed to describe the neuronal mechanisms underlying the transient modulation of cortical target circuits by cholinergic activity. These models postulate specific locations and roles of nicotinic and muscarinic acetylcholine receptors and that cholinergic neurotransmission is controlled in part by (cortical) target circuits. The available evidence and these models point to new principles governing the development of the next generation of cholinergic treatments for cognitive disorders.

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Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons.

Wyeth Bair, R. Cavanaugh, J. Movshon (2002)

Information is integrated across the visual field to transform local features into a global percept. We now know that V1 neurons provide more spatial integration than originally thought due to the existence of their nonclassical inhibitory surrounds. To understand spatial integration in the visual cortex, we have studied the nature and extent of center and surround influences on neuronal response. We used drifting sinusoidal gratings in circular and annular apertures to estimate the sizes of the receptive field's excitatory center and suppressive surround. We used combinations of stimuli inside and outside the receptive field to explore the nature of the surround influence on the receptive field center as a function of the relative and absolute contrast of stimuli in the two regions. We conclude that the interaction is best explained as a divisive modulation of response gain by signals from the surround. We then develop a receptive field model based on the ratio of signals from Gaussian-shaped center and surround mechanisms. We show that this model can account well for the variations in receptive field size with contrast that we and others have observed and for variations in size with the state of contrast adaptation. The model achieves this success by simple variations in the relative gain of the two component mechanisms of the receptive field. This model thus offers a parsimonious explanation of a variety of phenomena involving changes in apparent receptive field size and accounts for these phenomena purely in terms of two receptive field mechanisms that do not themselves change in size. We used the extent of the center mechanism in our model as an indicator of the spatial extent of the central excitatory portion of the receptive field. We compared the extent of the center to measurements of horizontal connections within V1 and determined that horizontal intracortical connections are well matched in extent to the receptive field center mechanism. Input to the suppressive surround may come in part from feedback signals from higher areas.

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Author and article information

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Alexander Thiele: alex.thiele@ncl.ac.uk

Journal

Journal ID (nlm-ta): Sci Rep

Journal ID (iso-abbrev): Sci Rep

Title: Scientific Reports

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2045-2322

Publication date (Electronic): 16 April 2021

Publication date PMC-release: 16 April 2021

Publication date Collection: 2021

Volume: 11

Electronic Location Identifier: 8384

Affiliations

[1 ]GRID grid.250903.d, ISNI 0000 0000 9566 0634, Feinstein Institute of Medical Research, ; New York, USA

[2 ]GRID grid.1006.7, ISNI 0000 0001 0462 7212, Biosciences Institute, Newcastle University, ; Henry Wellcome Building, Newcastle upon Tyne, NE2 4HH UK

Article

Publisher ID: 88044

DOI: 10.1038/s41598-021-88044-7

PMC ID: 8052350

PubMed ID: 33863988

SO-VID: ffbb5401-2100-4005-ad84-d7029c82876a

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 21 July 2020

Date accepted : 5 April 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100004440, Wellcome Trust;

Award ID: 070380/z/03/z

Award Recipient : Alexander Thiele

Funded by: FundRef http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;

Award ID: BBS/B/09325

Award Recipient : Alexander Thiele

Funded by: FundRef http://dx.doi.org/10.13039/501100000265, Medical Research Council;

Award ID: G0700976

Award Recipient : Alexander Thiele

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ScienceOpen disciplines: Uncategorized

Keywords: cellular neuroscience,visual system

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ScienceOpen disciplines: Uncategorized

Keywords: cellular neuroscience, visual system

Effects of muscarinic and nicotinic receptors on contextual modulation in macaque area V1

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Most cited references 67

Uncertainty, neuromodulation, and attention.

Modes and models of forebrain cholinergic neuromodulation of cognition.

Nature and interaction of signals from the receptive field center and surround in macaque V1 neurons.

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