Cited by 314Neural and Behavioral Psychology StudiesVisual perception and processing mechanismsNeural dynamics and brain function

The DOI matches its Crossref record; 55 of the 60 references it cites were found in a registry or an index; none of the 31 sources its claims cite is checked for support yet.

Reward Value-Based Gain Control: Divisive Normalization in Parietal Cortex

Open access

Louie, K., Grattan, L. E., Glimcher, P. W.·2011·Journal of Neuroscience

DOI 10.1523/jneurosci.1237-11.2011PMC PMC3285508

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Abstract

The representation of value is a critical component of decision making. Rational choice theory assumes that options are assigned absolute values, independent of the value or existence of other alternatives. However, context-dependent choice behavior in both animals and humans violates this assumption, suggesting that biological decision processes rely on comparative evaluation. Here we show that neurons in the monkey lateral intraparietal cortex encode a relative form of saccadic value, explicitly dependent on the values of the other available alternatives. Analogous to extra-classical receptive field effects in visual cortex, this relative representation incorporates target values outside the response field and is observed in both stimulus-driven activity and baseline firing rates. This context-dependent modulation is precisely described by divisive normalization, indicating that this standard form of sensory gain control may be a general mechanism of cortical computation. Such normalization in decision circuits effectively implements an adaptive gain control for value coding and provides a possible mechanistic basis for behavioral context-dependent violations of rationality.

AI snapshot

Written from the paper’s full text.

TL;DR

Neurons in monkey lateral intraparietal cortex (LIP) encode saccadic value relative to the values of other available alternatives, not as absolute values. Full divisive normalization best describes this context-dependent modulation, suggesting a canonical cortical gain-control mechanism for value coding.

Key findings

In a two-target task, LIP activity increased with reward inside the response field (Vin) and decreased with reward outside it (Vout): 12/16 neurons (75.0%) were positively correlated with Vin, and 18/27 (66.7%) were negatively correlated with Vout; population mean correlations were 0.33 and −0.21, respectively.
In a three-target task, stimulus-driven activity was suppressed by summed extra-RF value: 33/62 neurons (53.2%) were modulated, with 30/33 showing suppression; population mean correlation was −0.155 (p = 2.6×10−6). Activity in the absence of an RF target was also suppressed: 27/62 (43.6%) modulated, 21/27 suppressed; mean correlation −0.087 (p = 0.0019).
Full divisive normalization best fit individual neurons (MED-RF: 53/62, 85.5%; HIGH-RF: 16/17, 94.1%; LOW-RF: 26/41, 61.9%) and the combined population dataset (R² = 0.961) versus fractional (0.730), difference (0.601), and simple normalization (0.219); it also had the lowest cross-validated mean squared error (0.0393).
Suppression depended on extra-RF target value but not relative target distance (ANCOVA: value p = 0.004; distance p = 0.058; interaction p = 0.793), and behavioral measures such as fixation breaks, error rates, and reaction times showed no consistent dependence on Vout.

Methods

Three male rhesus monkeys performed two-target and three-target saccade tasks with water reward magnitudes assigned to targets inside or outside the LIP neuron’s response field. Two-target task: 27 LIP neurons (monkey D n = 17; monkey W n = 10), with a subset (n = 16) also tested with RF value varied. Three-target task: 62 neurons under MED-RF (monkey W n = 31; monkey B n = 31), plus 45 neurons under HIGH-RF or LOW-RF conditions.
Single-unit electrophysiology in LIP; activity analyzed mainly 0–1000 ms after peripheral target presentation and normalized to peak firing in single-target RF mapping trials.
Analyses included Pearson correlations, multiple regression with Vout and saccade latency, ANCOVA on a suppression index, and model fitting of fractional, difference, simple normalization, and full normalization models using AIC and leave-one-out cross-validation.

Limitations

Stated: the circuit mechanisms generating divisive normalization remain unknown, the biophysical implementation of the semisaturation term σ is unknown, and the causal role of normalized value coding in context-dependent choice remains to be explored.
Stated: visuospatial parameters may influence suppression when alternative targets are very close to the RF (distance effect p = 0.058, not significant here), and attention cannot be fully excluded as an alternative explanation, though the authors argue the parametric value effects are not easily reconciled with simple attentional modulation.
Evident: findings are restricted to macaque LIP, specific saccade tasks, and water reward magnitudes; some neurons were recorded under multiple value conditions, so across-condition analyses were restricted to population responses rather than individual-neuron comparisons.

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Integrity signals

Registry

Crossref · 10.1523/jneurosci.1237-11.2011

Cites

55 of 55 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

0 of 31 cited sources checked · 0 supported · 0 flagged

A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“In contrast, the average correlation coefficient in RF target-absent trials remained significantly negative.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As shown in Figure 5, population activity in the three-target task also depended on the value of the RF target, with progressively higher firing rates at larger levels of Vin.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Across the population of neurons, the average correlation coefficient was significantly negative for most of the cue presentation interval in both RF target-present and RF target-absent conditions (p < 0.05, t-test).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As shown for the example neuron in Figure 2B, activity in trials without a target in the RF also varied as a function of Vout (r = −0.161, p = 0.037).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibratedSingle case
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“We observed that stimulus-driven activity, elicited by the appearance of the target in the RF, was a consistent function of the total amount of reward available, despite the fact that RF target value remained constant.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.

Show all 56 claims

It may state two separate claims as one. 37
Probably not a substantial claim. 11

A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“The majority of LIP neurons were modulated by value context, with almost all neurons showing suppression (modulation: n = 33/62, 53.2%; suppression n = 30/33, 90.9%); furthermore, suppression was significant across the population of neurons (mean correlation −0.155; p = 2.6×10−6, t-test) and evident in the mean population activity (Figure 2C).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibratedn = 33
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“As shown in Figure 3, the population of LIP neurons displayed Vout-dependent suppression in both RF target-present and RF target-absent conditions across much of the trial, with peak modulation occurring approximately 200–300 ms after peripheral target onset.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Of the recorded neurons, firing rate was significantly dependent on only value in 29 neurons, on both value and latency in 3 neurons, and on only latency in 1 neuron, suggesting that the observed modulation of LIP activity was primarily driven by the value context.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:hedged· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“This value modulation in the absence of RF stimulation was significant for a large fraction of LIP neurons (modulation n = 27/62, 43.6%; suppression 21/27, 77.8%) and significant across the population (mean correlation −0.087; p = 0.0019, t-test).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibratedn = 27
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Despite constant Vin levels, activity in trials with a target in the RF (solid red symbols) was suppressed as Vout increased. Similarly, in trials without a target in the RF (solid blue symbols), activity decreased as a function of alternative target values.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“consistent with the timepoint analysis, average LIP activity is suppressed by Vout in RF target-absent conditions (mean r = −.0.071, p = 3.7×10−4) and unmodulated in RF target-present (mean r = 0.024, p = 0.302) conditions.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A result the paper reports from its own data — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Consistent with the results described above, increasing the value of the target outside the RF in the two-target conditions decreased LIP firing rates (red, orange). Furthermore, activity was also a function of target number, decreasing from single target (black) to double target (red, orange) to triple target (yellow) conditions.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
None of the sources cited for this claim have been checked yet.
In the paper
“Targets at these locations did not activate the recorded neuron when presented alone, consistent with a contralateral visual bias in LIP (Ben Hamed et al., 2001; Patel et al., 2010).”
§ Value-based gain control: divisive normalization in parietal cortex > DISCUSSION
What the sources say
- Not checked yetcites Ben Hamed et al., 2001
- Not checked yetcites Patel et al., 2010
Load-bearingStrength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
In the paper
“More recently, motivated by computational models of two-alternative choice behavior, some researchers have suggested that the difference in option values may better describe LIP activity (Corrado et al., 2005).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Divisive normalization and value coding
What the sources say
- Not checked yetcites Corrado et al., 2005
Strength:hedged· not yet calibratedCausal:correlational· not yet calibrated
Tests✗ Asserted: fails✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The authors may not put it forward as true. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Together, these results suggest that LIP encodes a context-dependent value representation, where the value configuration of the entire choice set controls both stimulus-driven and target-absent activity early in the valuation process.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Three-alternative neural data
Load-bearingStrength:hedged· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
None of the sources cited for this claim have been checked yet.
In the paper
“Early models of striate cortex described visual neuron function as a linear operation, producing responses that are weighted sums of relevant inputs (Hubel and Wiesel, 1962, 1968; Movshon et al., 1978).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Divisive normalization and value coding
What the sources say
- Not checked yetcites Hubel and Wiesel, 1962, 1968
- Not checked yetcites Movshon et al., 1978
Strength:plain· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
None of the sources cited for this claim have been checked yet.
In the paper
“Initial studies of value coding in LIP (Platt and Glimcher, 1999; Sugrue et al., 2004) focused on a fractional representation of value due to its association with classic matching law behavior (Herrnstein, 1961).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Divisive normalization and value coding
What the sources say
- Not checked yetcites Platt and Glimcher, 1999
- Not checked yetcites Sugrue et al., 2004
- Not checked yetcites Herrnstein, 1961
Strength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Analogous to extra-classical receptive field effects in visual cortex, this relative representation incorporates target values outside the response field and is observed in both stimulus-driven activity and baseline firing rates.”
§ Value-based gain control: divisive normalization in parietal cortex > Abstract
Load-bearingStrength:plain· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
A conclusion the paper draws from its own results — it cites no other source for it, so there is none to check. The quote shows it is in the paper.
In the paper
“Thus, activity was both an increasing function of Vin and a decreasing function of Vout, suggesting that LIP value representation is relative rather than absolute; we explore the specific algorithm underlying this relative representation below.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Two-alternative neural data
Load-bearingStrength:hedged· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
It may state two separate claims as one.
- The authors state this as an assumption: The value of a given target is equated with the associated reward magnitude.
None of the sources cited for this claim have been checked yet.
In the paper
“Furthermore, normalization-style models yield efficient coding of natural signal statistics in both visual and auditory modalities (Schwartz and Simoncelli, 2001; Valerio and Navarro, 2003) and may play a role in attentional processing (Reynolds et al., 1999; Reynolds and Heeger, 2009), suggesting that divisive normalization may serve as a canonical computational algorithm in cortical circuits.”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Divisive normalization and value coding
What the sources say
- Not checked yetcites Schwartz and Simoncelli, 2001
- Not checked yetcites Valerio and Navarro, 2003
- Not checked yetcites Reynolds and Heeger, 2009
Strength:hedged· not yet calibratedCausal:conditional· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it. It may state two separate claims as one.
None of the sources cited for this claim have been checked yet.
In the paper
“In sensory cortices, stimuli outside the classical receptive field can nonetheless significantly modulate neuronal activity. Many of these extra-classical effects are well-described by models where response is specified by the sensory properties of the stimulus inside the receptive field, divided by the weighted sum of the sensory properties of stimuli both outside and inside the receptive field (”
§ Value-based gain control: divisive normalization in parietal cortex > INTRODUCTION
What the sources say
- Not checked yetcites Heeger, 1992
- Not checked yetcites Carandini et al., 1997
- Not checked yetcites Cavanaugh et al., 2002
Load-bearingStrength:boosted· not yet calibratedCausal:correlational· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
Probably not a substantial claim. It may state two separate claims as one.
In the paper
“To address these issues, Heeger proposed that visual cortical function involves a normalization stage, where a given cell’s response is divided by a quantity representing the pooled activity of a large number of other similar neurons (Heeger, 1992).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Divisive normalization and value coding
What the sources say
- Not checked yetcites Heeger, 1992
Load-bearingStrength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✓ Load-bearing: passes✓ Based: passes
Probably not a substantial claim.
None of the sources cited for this claim have been checked yet.
In the paper
“This divisive normalization model explains a number of nonlinear phenomena in striate and extrastriate cortex (Carandini et al., 1997; Britten and Heuer, 1999; Cavanaugh et al., 2002; Heuer and Britten, 2002) as well as responses in the ventral visual stream (Zoccolan et al., 2005).”
§ Value-based gain control: divisive normalization in parietal cortex > RESULTS > Divisive normalization and value coding
What the sources say
- Not checked yetcites Carandini et al., 1997
- Not checked yetcites Britten and Heuer, 1999
- Not checked yetcites Cavanaugh et al., 2002
Strength:plain· not yet calibratedCausal:direct· not yet calibrated
Tests✓ Asserted: passes✓ Checkable: passes✗ Load-bearing: fails✓ Based: passes
Probably not a substantial claim. The paper’s conclusions may not depend on it.

45 of 45

The paper relies on this without support.
The neural basis of context-dependent valuation is unknown.
“However, the neural basis of such context-dependent valuation is unknown.”
The paper relies on this without support.
The specific form of value representation in LIP and how it arises out of cortical circuit interactions remains largely unexplored.
“Current evidence suggests that parietal neurons are modulated by the value of their associated saccade, but the specific form of value representation and how it arises out of cortical circuit interactions remains largely unexplored.”
The paper relies on this without support.
LIP neurons have a circumscribed response field and many have a similarly tuned response to upcoming saccade amplitude and direction.
“LIP neurons, like those in visual cortex, respond to stimulus presentation in a circumscribed region of visual space termed the response field (RF); many of these neurons also possess a similarly tuned response to upcoming saccade amplitude and direction.”
The authors state this as an assumption.
The value of a given target is equated with the associated reward magnitude.
“The value of a given target was equated with the associated reward magnitude.”

4 of 4

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Statistics recomputed

Every reported test result, recomputed from its test statistic and degrees of freedom. A result shows as not adding up only once an independent check has confirmed it.

Consistentχ²(4) = 5.6reported p = .23 · recomputed p = .231
“χ2(4) = 5.6, p = .23”
Consistentχ²(4) = 20.6reported p = .0004 · recomputed p < .001
“χ2(4) = 20.6, p = .0004”
Consistentχ²(4) = 4.5reported p = .34 · recomputed p = .343
“χ2(4) = 4.5, p = .34”
Consistentχ²(4) = 14.4reported p = .006 · recomputed p = .006
“χ2(4) = 14.4, p = .006”
Consistentχ²(3) = 13.4reported p = .004 · recomputed p = .004
“χ2(3) = 13.4, p = .004”
Consistentχ²(3) = 17.2reported p = .0006 · recomputed p < .001
“χ2(3) = 17.2, p = .0006”

6 of 6

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

LOW-RF neuron percentage does not match its count
Minor
The reported 26 of 41 neurons is 63.4%, not 61.9%.
Reported 61.9 · recomputed 63.414634

1 of 1

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“Reward Value-Based Gain Control: Divisive Normalization in”
Background
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Background
Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4
Reynolds, J. H., Chelazzi, L., & Desimone, R. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-05-01736.1999 · Cited by 1,236 · cited 2×
“Furthermore, normalization-style models yield efficient coding of natural signal statistics in both visual and auditory modalities (Schwartz and Simoncelli, 2001; Valerio and Navarro, 2003) and may play a role in attentional processing (Reynolds et al., 1999; Reynolds and Heeger, 2009), suggesting that divisive normal…”
BackgroundMethod
Effects of Attention on Orientation-Tuning Functions of Single Neurons in Macaque Cortical Area V4
McAdams, C. J., & Maunsell, J. H. R. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00431.1999 · Cited by 1,218 · cited 1×
“…modulation in visual cortices instead show a binary change in modulation when spatial attention is cued either to the RF or outside the RF (Motter, 1993; McAdams and Maunsell, 1999; Bisley and Goldberg, 2003), consistent with a stepwise effect of attentional allocation on neuronal responses.”
Background
Focal attention produces spatially selective processing in visual cortical areas V1, V2, and V4 in the presence of competing stimuli
Motter, B. C. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.70.3.909 · Cited by 1,055 · cited 1×
“…modulation in visual cortices instead show a binary change in modulation when spatial attention is cued either to the RF or outside the RF (Motter, 1993; McAdams and Maunsell, 1999; Bisley and Goldberg, 2003), consistent with a stepwise effect of attentional allocation on neuronal…”
Background
Attention, intention, and priority in the parietal lobe
Bisley, J. W., & Goldberg, M. E. (2010) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-060909-152823 · Cited by 1,043 · cited 2×
“In addition to responses related to target selection and action value, LIP neurons also show activity associated with the allocation of covert attention, driven by intrinsic visual salience or task relevance (Bisley and Goldberg, 2003, 2010; Oristaglio et al., 2006).”
Background
Matching Behavior and the Representation of Value in the Parietal Cortex
Sugrue, L. P., Corrado, G. S., & Newsome, W. T. (2004) · Science · doi:10.1126/science.1094765 · Cited by 1,030 · cited 8×
“Previous studies have framed LIP activity in terms of gain ratio (Platt and Glimcher, 1999) or fractional income (Sugrue et al., 2004; Corrado et al., 2005), both of which assume a fractional reward representation based on V in / (Vin Vout), but no study has isolated the effect of manipulating…”
BackgroundResultInfluential
The statistical reliability of signals in single neurons in cat and monkey visual cortex
Tolhurst, D. J., Movshon, J. A., & Dean, A. F. (1983) · Vision Research · doi:10.1016/0042-6989(83)90200-6 · Cited by 1,002 · cited 1×
“Cortical neurons exhibit considerable variability in their spiking activity, and information is likely represented by distributions of neurons and spiking rates (Tolhurst et al., 1983; Shadlen and Newsome, 1998; Pouget et al., 2003).”
Background
Linearity and Normalization in Simple Cells of the Macaque Primary Visual Cortex
Carandini, M., Heeger, D. J., & Movshon, J. A. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-21-08621.1997 · Cited by 926 · cited 7×
“…well described by models in which response is specified by the sensory properties of the stimulus inside the receptive field, divided by the weighted sum of the sensory properties of stimuli both outside and inside the receptive field (Heeger, 1992; Carandini et al., 1997; Cavanaugh et al., 2002).”
BackgroundInfluential
Spatial summation in the receptive fields of simple cells in the cat's striate cortex.
Movshon, J. A., Thompson, I. D., & Tolhurst, D. J. (1978) · The Journal of Physiology · doi:10.1113/jphysiol.1978.sp012488 · Cited by 890 · cited 1×
“Early models of striate cortex described visual neuron function as a linear operation, producing responses that are weighted sums of relevant inputs (Hubel and Wiesel, 1962, 1968; Movshon et al., 1978).”
Background
Natural signal statistics and sensory gain control
Schwartz, O., & Simoncelli, E. P. (2001) · Nature Neuroscience · doi:10.1038/90526 · Cited by 835 · cited 3×
“…divisive inhibition has been shown to increase the independence of neural responses and allow for efficient encoding of sensory signals (Schwartz and Simoncelli, 2001) and to enhance the stability of recurrent neural networks (Chance and Abbott, 2000), leading to the idea that divisive…”
BackgroundMethod
Neuronal Activity in the Lateral Intraparietal Area and Spatial Attention
Bisley, J. W., & Goldberg, M. E. (2003) · Science · doi:10.1126/science.1077395 · Cited by 821
Increased Attention Enhances Both Behavioral and Neuronal Performance
Spitzer, H., Desimone, R., & Moran, J. (1988) · Science · doi:10.1126/science.3353728 · Cited by 815 · cited 1×
“Although there exists some evidence from tasks varying task difficulty that attentional modulation may be graded (Spitzer et al., 1988; Chen et al., 2008), no previous evidence exists for such a continuous, parametric effect of attention on neuronal responses.”
Background
Nature and Interaction of Signals From the Receptive Field Center and Surround in Macaque V1 Neurons
Cavanaugh, J. R., Bair, W., & Movshon, J. A. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00692.2001 · Cited by 784 · cited 6×
“…well described by models in which response is specified by the sensory properties of the stimulus inside the receptive field, divided by the weighted sum of the sensory properties of stimuli both outside and inside the receptive field (Heeger, 1992; Carandini et al., 1997; Cavanaugh et al., 2002).”
BackgroundInfluential
Decision-making with multiple alternatives
Churchland, A. K., Kiani, R., & Shadlen, M. N. (2008) · Nature Neuroscience · doi:10.1038/nn.2123 · Cited by 671 · cited 1×
“Similarly, in a motion-discrimination task with varying numbers of alternatives, LIP activity is lower when four choices are presented rather than two choices (Churchland et al., 2008).”
Background
Summation and Division by Neurons in Primate Visual Cortex
Carandini, M., & Heeger, D. J. (1994) · Science · doi:10.1126/science.8191289 · Cited by 649 · cited 2×
“Normalization characterizes stimulus interaction within the V1 RF (Carandini and Heeger, 1994; Carandini et al., 1997), as well as interactions between the RF center and nonclassical suppressive surround (Cavanaugh et al.”
Background
Neural Activity in Macaque Parietal Cortex Reflects Temporal Integration of Visual Motion Signals during Perceptual Decision Making
Huk, A. C., & Shadlen, M. N. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.4684-04.2005 · Cited by 538 · cited 2×
“Reward Value-Based Gain Control: Divisive Normalization in”
Background
Modulation of Neuronal Activity in Superior Colliculus by Changes in Target Probability
Basso, M. A., & Wurtz, R. H. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-18-07519.1998 · Cited by 474 · cited 2×
“One important prediction of the normalization model is that modulation by the number of alternatives should reflect not simple set size but the underlying effect of target uncertainty on value; such a relationship exists in the superior colliculus, where target uncertainty mediates the inverse relationship between the…”
Background
I NFERENCE AND C OMPUTATION WITH P OPULATION C ODES
Pouget, A., Dayan, P., & Zemel, R. S. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131112 · Cited by 446 · cited 1×
“Cortical neurons exhibit considerable variability in their spiking activity, and information is likely represented by distributions of neurons and spiking rates (Tolhurst et al., 1983; Shadlen and Newsome, 1998; Pouget et al., 2003).”
Background
Activity in Posterior Parietal Cortex Is Correlated with the Relative Subjective Desirability of Action
Dorris, M. C., & Glimcher, P. W. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.009 · Cited by 440 · cited 2×
“Reward Value-Based Gain Control: Divisive Normalization in”
BackgroundSelf-citation
Neuronal representations of cognitive state: reward or attention?
Maunsell, J. H. R. (2004) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2004.04.003 · Cited by 404 · cited 1×
“Reward- and attention-based effects on neural activity are difficult to dissociate (Maunsell, 2004), raising the possibility that value-guided normalization may be itself mediated by attentional processes, with less attention allocated to the RF location as alternative values increase.”
Background
Context-dependent violations of rational choice in honeybees ( Apis mellifera ) and gray jays ( Perisoreus canadensis )
Shafir, S., Waite, T. A., & Smith, B. H. (2002) · Behavioral Ecology and Sociobiology · doi:10.1007/s00265-001-0420-8 · Cited by 272 · cited 2×
“…additive noise or correlated activity) could decrease the discriminability between the options as the distributions are normalized, leading to stochastic choice behavior that is dependent on the composition of the choice set (Tversky and Simonson, 1993; Shafir et al., 2002; Bateson et al., 2003).”
Background
Task difficulty modulates the activity of specific neuronal populations in primary visual cortex
Chen, Y., Martínez‐Conde, S., Macknik, S. L., Bereshpolova, Y., Swadlow, H. A., & Alonso, J. (2008) · Nature Neuroscience · doi:10.1038/nn.2147 · Cited by 253 · cited 1×
“Although there exists some evidence from tasks varying task difficulty that attentional modulation may be graded (Spitzer et al., 1988; Chen et al., 2008), no previous evidence exists for such a continuous, parametric effect of attention on neuronal responses.”
Background
Representation of Concurrent Stimuli by Population Activity in Visual Cortex
Busse, L., Wade, A. R., & Carandini, M. (2009) · Neuron · doi:10.1016/j.neuron.2009.11.004 · Cited by 247 · cited 2×
“…interaction within the V1 RF (Carandini and Heeger, 1994; Carandini et al., 1997), as well as interactions between the RF center and nonclassical suppressive surround (Cavanaugh et al., 2002), and governs both single neuron and population responses (Busse et al., 2009; MacEvoy et al., 2009).”
Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis
Ben Hamed, S., Duhamel, J.-R., Bremmer, F., & Graf, W. (2001) · Experimental Brain Research · doi:10.1007/s002210100785 · Cited by 242 · cited 1×
“Targets at these locations did not activate the recorded neuron when presented alone, consistent with a contralateral visual bias in LIP (Ben Hamed et al., 2001; Patel et al., 2010).”
Background
Multiple Object Response Normalization in Monkey Inferotemporal Cortex
Zoccolan, D., Cox, D., & DiCarlo, J. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2058-05.2005 · Cited by 227 · cited 3×
“This divisive normalization model explains a number of nonlinear phenomena in striate and extrastriate cortex (Carandini et al., 1997; Britten and Heuer, 1999; Cavanaugh et al., 2002; Heuer and Britten, 2002) as well as responses in the ventral visual stream (Zoccolan et al., 2005).”
Background
LINEAR-NONLINEAR-POISSON MODELS OF PRIMATE CHOICE DYNAMICS
Corrado, G. S., Sugrue, L. P., Seung, H. S., & Newsome, W. T. (2005) · Journal of the Experimental Analysis of Behavior · doi:10.1901/jeab.2005.23-05 · Cited by 206
Spatial Summation in the Receptive Fields of MT Neurons
Britten, K. H., & Heuer, H. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-12-05074.1999 · Cited by 200 · cited 3×
“This divisive normalization model explains a number of nonlinear phenomena in striate and extrastriate cortex (Carandini et al., 1997; Britten and Heuer, 1999; Cavanaugh et al., 2002; Heuer and Britten, 2002) as well as responses in the ventral visual stream (Zoccolan et al.”
Background
Responses of Intraparietal Neurons to Saccadic Targets and Visual Distractors
Platt, M. L., & Glimcher, P. W. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.78.3.1574 · Cited by 194 · cited 1×
“Experiments were conducted in a dimly lit, sound-attenuated room using standard techniques (Platt and Glimcher, 1997).”
MethodSelf-citation
Separating Value from Choice: Delay Discounting Activity in the Lateral Intraparietal Area
Louie, K., & Glimcher, P. W. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.5742-09.2010 · Cited by 192 · cited 1×
“These temporal dynamics are consistent with the timing of value representation in LIP, which predominates early in the decision process but is eventually outweighed by the representation of choice (Platt and Glimcher, 1999; Louie and Glimcher, 2010).”
BackgroundSelf-citation
Context–dependent foraging decisions in rufous hummingbirds
Bateson, M., Healy, S. D., & Hurly, T. A. (2003) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2003.2365 · Cited by 182 · cited 2×
“…additive noise or correlated activity) could decrease the discriminability between the options as the distributions are normalized, leading to stochastic choice behavior that is dependent on the composition of the choice set (Tversky and Simonson, 1993; Shafir et al., 2002; Bateson et al., 2003).”
Background
A Canonical Neural Circuit for Cortical Nonlinear Operations
Kouh, M., & Poggio, T. (2008) · Neural Computation · doi:10.1162/neco.2008.02-07-466 · Cited by 165 · cited 1×
“…in value coding, the circuit mechanisms generating this representation remain unknown; such computations may emerge from fundamental properties of the neural circuit architecture (Kouh and Poggio, 2008), and identifying the underlying mechanism remains a critical direction for future work.”
Background
Spatial Attention Modulates Center-Surround Interactions in Macaque Visual Area V4
Sundberg, K. A., Mitchell, J. F., & Reynolds, J. H. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.023 · Cited by 157 · cited 1×
“This idea is supported by recent recordings in V4, in which attention modulates the gain of existing center-surround interactions, with increased suppression of RF activity when attention is directed toward stimuli in the RF surround (Sundberg et al., 2009).”
Contrast Dependence of Response Normalization in Area MT of the Rhesus Macaque
Heuer, H. W., & Britten, K. H. (2002) · Journal of Neurophysiology · doi:10.1152/jn.00255.2002 · Cited by 136 · cited 3×
“This divisive normalization model explains a number of nonlinear phenomena in striate and extrastriate cortex (Carandini et al., 1997; Britten and Heuer, 1999; Cavanaugh et al., 2002; Heuer and Britten, 2002) as well as responses in the ventral visual stream (Zoccolan et al.”
Background
Lateral Intraparietal Cortex and Reinforcement Learning during a Mixed-Strategy Game
Seo, H., Barraclough, D. J., & Lee, D. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.1479-09.2009 · Cited by 125 · cited 2×
“Reward Value-Based Gain Control: Divisive Normalization in”
Background
Neural Correlates of Attention and Distractibility in the Lateral Intraparietal Area
Bisley, J. W., & Goldberg, M. E. (2005) · Journal of Neurophysiology · doi:10.1152/jn.00848.2005 · Cited by 122 · cited 1×
“Finally, when attention and parietal activity are examined together, LIP appears to specify the locus of attention rather than vary parametrically with the behavioral attentional advantage (Bisley and Goldberg, 2003, 2006).”
Background
Integration of visuospatial and effector information during symbolically cued limb movements in monkey lateral intraparietal area
Oristaglio, J., Schneider, D. M., Balan, P. F., & Gottlieb, J. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1779-06.2006 · Cited by 102 · cited 1×
“In addition to responses related to target selection and action value, LIP neurons also show activity associated with the allocation of covert attention, driven by intrinsic visual salience or task relevance (Bisley and Goldberg, 2003, 2010; Oristaglio et al., 2006).”
Background
Neuronal correlates of the set-size effect in monkey lateral intraparietal area
Balan, P. F., Oristaglio, J., Schneider, D. M., & Gottlieb, J. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060158 · Cited by 83 · cited 1×
“In a covert visual search task, LIP neurons show graded activity that declines with the number of presented distractors (Balan et al., 2008).”
Background
Topographic organization of macaque area LIP
Patel, G. H., Shulman, G. L., Baker, J. T., Akbudak, E., Snyder, A. Z., Snyder, L. H., & Corbetta, M. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908092107 · Cited by 73 · cited 1×
“Targets at these locations did not activate the recorded neuron when presented alone, consistent with a contralateral visual bias in LIP (Ben Hamed et al., 2001; Patel et al., 2010).”
Background
A precise form of divisive suppression supports population coding in the primary visual cortex
MacEvoy, S. P., Tucker, T. R., & Fitzpatrick, D. (2009) · Nature Neuroscience · doi:10.1038/nn.2310 · Cited by 64 · cited 2×
“…interaction within the V1 RF (Carandini and Heeger, 1994; Carandini et al., 1997), as well as interactions between the RF center and nonclassical suppressive surround (Cavanaugh et al., 2002), and governs both single neuron and population responses (Busse et al., 2009; MacEvoy et al., 2009).”
Background
Divisive inhibition in recurrent networks
Chance, F. S., & Abbott, L. F. (2000) · Network Computation in Neural Systems · doi:10.1088/0954-898x_11_2_301 · Cited by 49 · cited 1×
“…of neural responses and allow for efficient encoding of sensory signals (Schwartz and Simoncelli, 2001) and to enhance the stability of recurrent neural networks (Chance and Abbott, 2000), leading to the idea that divisive normalization may be a canonical computation of cortical circuits.”
Background
Context-Dependent Preferences
Tversky, A., & Simonson, I. (2000) · Cambridge University Press eBooks · doi:10.1017/cbo9780511803475.030 · Cited by 32
Optimal coding through divisive normalization models of V1 neurons
Valerio, R., & Navarro, R. (2003) · Network Computation in Neural Systems · doi:10.1088/0954-898x_14_3_310 · Cited by 22 · cited 2×
“…models yield efficient coding of natural signal statistics in both visual and auditory modalities (Schwartz and Simoncelli, 2001; Valerio and Navarro, 2003) and may play a role in attentional processing (Reynolds et al., 1999; Reynolds and Heeger, 2009), suggesting that divisive…”
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The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value
Bartra, O., McGuire, J. T., & Kable, J. W. (2013) · NeuroImage · doi:10.1016/j.neuroimage.2013.02.063 · Cited by 1,927
“We have assumed for simplicity that zero corresponds to no outcome at all, but there is evidence that decision makers actually evaluate outcomes relative to a reference point based either on predictions (Montague et al., 1996) or concurrent context (Louie et al., 2011).”
Normalization as a canonical neural computation
Carandini, M., & Heeger, D. J. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3136 · Cited by 1,906
Top-down versus bottom-up attentional control: a failed theoretical dichotomy
Awh, E., Belopolsky, A. V., & Theeuwes, J. (2012) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2012.06.010 · Cited by 1,557
Spectral fingerprints of large-scale neuronal interactions
Siegel, M., Donner, T. H., & Engel, A. K. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3137 · Cited by 1,295
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Schultz, W. (2015) · Physiological Reviews · doi:10.1152/physrev.00023.2014 · Cited by 1,126
“Divisive normalization from sensory physiology describes well the adaptations to changes in individual values of choice options in reward neurons of parietal cortex (332).”
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Authors: Louie, K., Grattan, L. E., & Glimcher, P. W.
Affiliations: New York University (US)
ORCID: Louie, K.
Grattan, L. E.
Glimcher, P. W.
Venue: Journal of Neuroscience
Publisher: Society for Neuroscience
Published: 2011-07-20
Volume: 31
Issue: 29
Pages: 10627-10639
ISSN: 0270-6474 (ISSN-L)
1529-2401
DOI: 10.1523/jneurosci.1237-11.2011
PMC: PMC3285508
OpenAlex: W2069815761
Semantic Scholar: 2c68a342adf5dd25439ef7f3f553afd1e9a0d1d4
Cited by: 308
References: 60
Citations by year: 2026: 7 · 2025: 13 · 2024: 20 · 2023: 22 · 2022: 18 · 2021: 29 · 2020: 19 · 2019: 25 · 2018: 23 · 2017: 22 · 2016: 16 · 2015: 24 · 2014: 23 · 2013: 24 · 2012: 19
FWCI: 11.36
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Journal of Neuroscience (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Eye Institute (R01EY010536)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords: divisive normalization, gain control, context-dependent choice, comparative analysis, decision-making, monkey visual cortex
MeSH terms: Action Potentials, Analysis of Variance, Animals, Choice Behavior, Macaca mulatta, Male, Models, Neurological, Neurons, Parietal Lobe, Photic Stimulation, Predictive Value of Tests, Reference Values, Reward, Time Factors, Chi-Square Distribution

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Reward Value-Based Gain Control: Divisive Normalization in Parietal Cortex

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