Literature DB >> 31068439

Neuronal Effects of Spatial and Feature Attention Differ Due to Normalization.

Amy M Ni1,2, John H R Maunsell3,4.   

Abstract

Although spatial and feature attention have differing effects on neuronal responses in visual cortex, it remains unclear why. Response normalization has been implicated in both types of attention (Carandini and Heeger, 2011), and single-unit studies have demonstrated that the magnitude of spatial attention effects on neuronal responses covaries with the magnitude of normalization effects. However, the relationship between feature attention and normalization remains largely unexplored. We recorded from individual neurons in the middle temporal area of rhesus monkeys using a task that allowed us to isolate the effects of feature attention, spatial attention, and normalization on the responses of each neuron. We found that the magnitudes of neuronal response modulations due to spatial attention and feature attention are correlated; however, whereas modulations due to spatial attention are correlated with normalization strength, those due to feature attention are not. Additionally, spatial attention modulations are stronger with multiple stimuli in the receptive field, whereas feature attention modulations are not. These findings are captured by a model in which spatial and feature attention share common top-down attention signals that nonetheless result in differing sensory neuron response modulations because of a spatially tuned sensory normalization mechanism. This model explains previously reported commonalities and differences between these two types of attention by clarifying the relationship between top-down attention signals and sensory normalization. We conclude that similar top-down signals to visual cortex can have distinct effects on neuronal responses due to distinct interactions with sensory mechanisms.SIGNIFICANCE STATEMENT Subjects use attention to improve their visual perception in several ways, including by attending to a location in space or to a visual feature. Prior studies have found both commonalities and differences between the effects of spatial and feature attention on neuronal responses in visual cortex, although it is unclear what mechanisms could explain this range of effects. Normalization, a computation by which neuronal responses are modified by stimulus context, has been implicated in many neuronal mechanisms throughout the brain. Here we propose that normalization provides a simple explanation for how spatial and feature attention could share common top-down attention signals that still affect sensory neuron responses differently.
Copyright © 2019 the authors.

Entities:  

Keywords:  feature attention; macaque; middle temporal; normalization; single unit; spatial attention

Mesh:

Year:  2019        PMID: 31068439      PMCID: PMC6616284          DOI: 10.1523/JNEUROSCI.2106-18.2019

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  68 in total

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Authors:  K H Britten; H W Heuer
Journal:  J Neurosci       Date:  1999-06-15       Impact factor: 6.167

2.  Feature-based attention influences motion processing gain in macaque visual cortex.

Authors:  S Treue; J C Martínez Trujillo
Journal:  Nature       Date:  1999-06-10       Impact factor: 49.962

3.  Attention to both space and feature modulates neuronal responses in macaque area V4.

Authors:  C J McAdams; J H Maunsell
Journal:  J Neurophysiol       Date:  2000-03       Impact factor: 2.714

Review 4.  Mechanisms of visual attention in the human cortex.

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Journal:  Annu Rev Neurosci       Date:  2000       Impact factor: 12.449

5.  A physiological correlate of the 'spotlight' of visual attention.

Authors:  J A Brefczynski; E A DeYoe
Journal:  Nat Neurosci       Date:  1999-04       Impact factor: 24.884

6.  Two-dimensional substructure of MT receptive fields.

Authors:  M S Livingstone; C C Pack; R T Born
Journal:  Neuron       Date:  2001-06       Impact factor: 17.173

7.  Contrast dependence of response normalization in area MT of the rhesus macaque.

Authors:  Hilary W Heuer; Kenneth H Britten
Journal:  J Neurophysiol       Date:  2002-12       Impact factor: 2.714

8.  Selective gating of visual signals by microstimulation of frontal cortex.

Authors:  Tirin Moore; Katherine M Armstrong
Journal:  Nature       Date:  2003-01-23       Impact factor: 49.962

9.  Normalization of cell responses in cat striate cortex.

Authors:  D J Heeger
Journal:  Vis Neurosci       Date:  1992-08       Impact factor: 3.241

10.  Global effects of feature-based attention in human visual cortex.

Authors:  Melissa Saenz; Giedrius T Buracas; Geoffrey M Boynton
Journal:  Nat Neurosci       Date:  2002-07       Impact factor: 24.884

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  10 in total

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Authors:  Douglas A Ruff; Cheng Xue; Lily E Kramer; Faisal Baqai; Marlene R Cohen
Journal:  Proc Natl Acad Sci U S A       Date:  2020-11-24       Impact factor: 11.205

2.  Understanding Commonalities and Discrepancies between Feature and Spatial Attention Effect in the Context of a Normalization Model.

Authors:  Yang Xie; Zhewei Zhang
Journal:  J Neurosci       Date:  2020-01-29       Impact factor: 6.167

3.  Differential Effects of Endogenous and Exogenous Attention on Sensory Tuning.

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4.  Pop-out search instigates beta-gated feature selectivity enhancement across V4 layers.

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5.  Choice-related activity and neural encoding in primary auditory cortex and lateral belt during feature-selective attention.

Authors:  Jennifer L Mohn; Joshua D Downer; Kevin N O'Connor; Jeffrey S Johnson; Mitchell L Sutter
Journal:  J Neurophysiol       Date:  2021-03-31       Impact factor: 2.714

6.  Different computations underlie overt presaccadic and covert spatial attention.

Authors:  Hsin-Hung Li; Jasmine Pan; Marisa Carrasco
Journal:  Nat Hum Behav       Date:  2021-04-19

Review 7.  To look or not to look: dissociating presaccadic and covert spatial attention.

Authors:  Hsin-Hung Li; Nina M Hanning; Marisa Carrasco
Journal:  Trends Neurosci       Date:  2021-06-04       Impact factor: 16.978

8.  Spatial and Feature-selective Attention Have Distinct, Interacting Effects on Population-level Tuning.

Authors:  Erin Goddard; Thomas A Carlson; Alexandra Woolgar
Journal:  J Cogn Neurosci       Date:  2022-01-05       Impact factor: 3.420

9.  Effect of Cross-Orientation Normalization on Different Neural Measures in Macaque Primary Visual Cortex.

Authors:  Aritra Das; Supratim Ray
Journal:  Cereb Cortex Commun       Date:  2021-02-10

10.  A dynamic normalization model of temporal attention.

Authors:  Rachel N Denison; Marisa Carrasco; David J Heeger
Journal:  Nat Hum Behav       Date:  2021-06-17
  10 in total

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