Diverse Neuronal Activity Patterns Contribute to the Control of Distraction in the Prefrontal and Parietal Cortex

Overview

Journal PLoS Biol

Date 2025 Jan 27

PMID 39869632

Authors

Panagiotis Sapountzis

Alexandra Antoniadou

Georgia G Gregoriou

Affiliations

Soon will be listed here.

Abstract

Goal-directed behavior requires the effective suppression of distractions to focus on the task at hand. Although experimental evidence suggests that brain areas in the prefrontal and parietal lobe contribute to the selection of task-relevant and the suppression of task-irrelevant stimuli, how conspicuous distractors are encoded and effectively ignored remains poorly understood. We recorded neuronal responses from 2 regions in the prefrontal and parietal cortex of macaques, the frontal eye field (FEF) and the lateral intraparietal (LIP) area, during a visual search task, in the presence and absence of a salient distractor. We found that in both areas, salient distractors are encoded by both response enhancement and suppression by distinct neuronal populations. In FEF, a larger proportion of units displayed suppression of responses to the salient distractor compared to LIP, with suppression effects in FEF being correlated with search time. Moreover, in FEF but not in LIP, the suppression for the salient distractor compared to non-salient distractors that shared the target color could not be accounted for by an enhancement of target features. These results reveal a distinct contribution of FEF in the suppression of salient distractors. Critically, we found that in both areas, the population level representations of the target and singleton locations were not orthogonal, suggesting a mechanism of interference from salient stimuli.

References

Sapountzis P, Gregoriou G . Neural signatures of attention: insights from decoding population activity patterns. Front Biosci (Landmark Ed). 2017; 23(2):221-246. DOI: 10.2741/4588. View

Parthasarathy A, Tang C, Herikstad R, Cheong L, Yen S, Libedinsky C . Time-invariant working memory representations in the presence of code-morphing in the lateral prefrontal cortex. Nat Commun. 2019; 10(1):4995. PMC: 6825148. DOI: 10.1038/s41467-019-12841-y. View

Barack D, Krakauer J . Two views on the cognitive brain. Nat Rev Neurosci. 2021; 22(6):359-371. DOI: 10.1038/s41583-021-00448-6. View

Asaad W, Santhanam N, McClellan S, Freedman D . High-performance execution of psychophysical tasks with complex visual stimuli in MATLAB. J Neurophysiol. 2012; 109(1):249-60. PMC: 3545163. DOI: 10.1152/jn.00527.2012. View

Gaspelin N, Luck S . The Role of Inhibition in Avoiding Distraction by Salient Stimuli. Trends Cogn Sci. 2017; 22(1):79-92. PMC: 5742040. DOI: 10.1016/j.tics.2017.11.001. View

Belopolsky A, Zwaan L, Theeuwes J, Kramer A . The size of an attentional window modulates attentional capture by color singletons. Psychon Bull Rev. 2007; 14(5):934-8. DOI: 10.3758/bf03194124. View

Klink P, Teeuwen R, Lorteije J, Roelfsema P . Inversion of pop-out for a distracting feature dimension in monkey visual cortex. Proc Natl Acad Sci U S A. 2023; 120(9):e2210839120. PMC: 9992771. DOI: 10.1073/pnas.2210839120. View

Olejnik S, Algina J . Generalized eta and omega squared statistics: measures of effect size for some common research designs. Psychol Methods. 2003; 8(4):434-47. DOI: 10.1037/1082-989X.8.4.434. View

Bichot N, Chenchal Rao S, Schall J . Continuous processing in macaque frontal cortex during visual search. Neuropsychologia. 2001; 39(9):972-82. DOI: 10.1016/s0028-3932(01)00022-7. View

10.

Zhou H, Desimone R . Feature-based attention in the frontal eye field and area V4 during visual search. Neuron. 2011; 70(6):1205-17. PMC: 3490686. DOI: 10.1016/j.neuron.2011.04.032. View

11.

Lien M, Ruthruff E, Johnston J . Attentional capture with rapidly changing attentional control settings. J Exp Psychol Hum Percept Perform. 2010; 36(1):1-16. DOI: 10.1037/a0015875. View

12.

Bichot N, Heard M, DeGennaro E, Desimone R . A Source for Feature-Based Attention in the Prefrontal Cortex. Neuron. 2015; 88(4):832-44. PMC: 4655197. DOI: 10.1016/j.neuron.2015.10.001. View

13.

Kerzel D, Burra N . Capture by Context Elements, Not Attentional Suppression of Distractors, Explains the P with Small Search Displays. J Cogn Neurosci. 2020; 32(6):1170-1183. DOI: 10.1162/jocn_a_01535. View

14.

Mendoza-Halliday D, Martinez-Trujillo J . Neuronal population coding of perceived and memorized visual features in the lateral prefrontal cortex. Nat Commun. 2017; 8:15471. PMC: 5461493. DOI: 10.1038/ncomms15471. View

15.

Kerzel D, Huynh Cong S, Burra N . Do we need attentional suppression?. Vis cogn. 2021; 29(9):580-582. PMC: 8547733. DOI: 10.1080/13506285.2021.1918304. View

16.

Oxner M, Martinovic J, Forschack N, Lempe R, Gundlach C, Muller M . Global enhancement of target color-not proactive suppression-explains attentional deployment during visual search. J Exp Psychol Gen. 2023; 152(6):1705-1722. DOI: 10.1037/xge0001350. View

17.

Tremblay S, Pieper F, Sachs A, Martinez-Trujillo J . Attentional filtering of visual information by neuronal ensembles in the primate lateral prefrontal cortex. Neuron. 2014; 85(1):202-215. DOI: 10.1016/j.neuron.2014.11.021. View

18.

Wang B, Theeuwes J . Salience determines attentional orienting in visual selection. J Exp Psychol Hum Percept Perform. 2020; 46(10):1051-1057. DOI: 10.1037/xhp0000796. View

19.

Buschman T, Siegel M, Roy J, Miller E . Neural substrates of cognitive capacity limitations. Proc Natl Acad Sci U S A. 2011; 108(27):11252-5. PMC: 3131328. DOI: 10.1073/pnas.1104666108. View

20.

Ma X, Abrams R . Feature-blind attentional suppression of salient distractors. Atten Percept Psychophys. 2023; 85(5):1409-1424. DOI: 10.3758/s13414-023-02712-6. View