Modulation of Neuronal Activity and Saccades at Theta Rhythm During Visual Search in Non-human Primates

Overview

Journal Neurosci Bull

Specialty Neurology

Date 2022 May 24

PMID 35608752

Authors

Jin Xie

Ting Yan

Jie Zhang

Zhengyu Ma

Huihui Zhou

Affiliations

Soon will be listed here.

Abstract

Active exploratory behaviors have often been associated with theta oscillations in rodents, while theta oscillations during active exploration in non-human primates are still not well understood. We recorded neural activities in the frontal eye field (FEF) and V4 simultaneously when monkeys performed a free-gaze visual search task. Saccades were strongly phase-locked to theta oscillations of V4 and FEF local field potentials, and the phase-locking was dependent on saccade direction. The spiking probability of V4 and FEF units was significantly modulated by the theta phase in addition to the time-locked modulation associated with the evoked response. V4 and FEF units showed significantly stronger responses following saccades initiated at their preferred phases. Granger causality and ridge regression analysis showed modulatory effects of theta oscillations on saccade timing. Together, our study suggests phase-locking of saccades to the theta modulation of neural activity in visual and oculomotor cortical areas, in addition to the theta phase locking caused by saccade-triggered responses.

Citing Articles

Orchestration of saccadic eye-movements by brain rhythms in macaque Frontal Eye Field.

Shaverdi Y, Setarehdan S, Treue S, Esghaei M Sci Rep. 2023; 13(1):22725.

PMID: 38123575 PMC: 10733338. DOI: 10.1038/s41598-023-49346-0.

References

Landau A, Schreyer H, van Pelt S, Fries P . Distributed Attention Is Implemented through Theta-Rhythmic Gamma Modulation. Curr Biol. 2015; 25(17):2332-7. DOI: 10.1016/j.cub.2015.07.048. View

Fiebelkorn I, Pinsk M, Kastner S . A Dynamic Interplay within the Frontoparietal Network Underlies Rhythmic Spatial Attention. Neuron. 2018; 99(4):842-853.e8. PMC: 6474777. DOI: 10.1016/j.neuron.2018.07.038. View

Confais J, Malfait N, Brochier T, Riehle A, Kilavik B . Is there an Intrinsic Relationship between LFP Beta Oscillation Amplitude and Firing Rate of Individual Neurons in Macaque Motor Cortex?. Cereb Cortex Commun. 2021; 1(1):tgaa017. PMC: 8152857. DOI: 10.1093/texcom/tgaa017. View

Buzsaki G . Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus. 2005; 15(7):827-40. DOI: 10.1002/hipo.20113. View

Grastyan E, Lissak K, MADARASZ I, DONHOFFER H . Hippocampal electrical activity during the development of conditioned reflexes. Electroencephalogr Clin Neurophysiol. 1959; 11(3):409-30. DOI: 10.1016/0013-4694(59)90040-9. View

Han H, Lee K, Choi J . Functional Dissociation of θ Oscillations in the Frontal and Visual Cortices and Their Long-Range Network during Sustained Attention. eNeuro. 2019; 6(6). PMC: 6860984. DOI: 10.1523/ENEURO.0248-19.2019. View

Yan T, Zhou H . Synchronization between frontal eye field and area V4 during free-gaze visual search. Zool Res. 2019; 40(5):394-403. PMC: 6755118. DOI: 10.24272/j.issn.2095-8137.2019.055. View

Jutras M, Fries P, Buffalo E . Oscillatory activity in the monkey hippocampus during visual exploration and memory formation. Proc Natl Acad Sci U S A. 2013; 110(32):13144-9. PMC: 3740906. DOI: 10.1073/pnas.1302351110. View

Ogawa T, Komatsu H . Target selection in area V4 during a multidimensional visual search task. J Neurosci. 2004; 24(28):6371-82. PMC: 6729540. DOI: 10.1523/JNEUROSCI.0569-04.2004. View

10.

Tort A, Kramer M, Thorn C, Gibson D, Kubota Y, Graybiel A . Dynamic cross-frequency couplings of local field potential oscillations in rat striatum and hippocampus during performance of a T-maze task. Proc Natl Acad Sci U S A. 2008; 105(51):20517-22. PMC: 2629291. DOI: 10.1073/pnas.0810524105. View

11.

Monosov I, Sheinberg D, Thompson K . Paired neuron recordings in the prefrontal and inferotemporal cortices reveal that spatial selection precedes object identification during visual search. Proc Natl Acad Sci U S A. 2010; 107(29):13105-10. PMC: 2919901. DOI: 10.1073/pnas.1002870107. View

12.

Killian N, Potter S, Buffalo E . Saccade direction encoding in the primate entorhinal cortex during visual exploration. Proc Natl Acad Sci U S A. 2015; 112(51):15743-8. PMC: 4697421. DOI: 10.1073/pnas.1417059112. View

13.

Fiebelkorn I, Pinsk M, Kastner S . The mediodorsal pulvinar coordinates the macaque fronto-parietal network during rhythmic spatial attention. Nat Commun. 2019; 10(1):215. PMC: 6333835. DOI: 10.1038/s41467-018-08151-4. View

14.

Schall J, Hanes D, Thompson K, King D . Saccade target selection in frontal eye field of macaque. I. Visual and premovement activation. J Neurosci. 1995; 15(10):6905-18. PMC: 6577995. View

15.

Bartlett A, Ovaysikia S, Logothetis N, Hoffman K . Saccades during object viewing modulate oscillatory phase in the superior temporal sulcus. J Neurosci. 2011; 31(50):18423-32. PMC: 6623894. DOI: 10.1523/JNEUROSCI.4102-11.2011. View

16.

Mazer J, Gallant J . Goal-related activity in V4 during free viewing visual search. Evidence for a ventral stream visual salience map. Neuron. 2003; 40(6):1241-50. DOI: 10.1016/s0896-6273(03)00764-5. View

17.

Schomburg E, Fernandez-Ruiz A, Mizuseki K, Berenyi A, Anastassiou C, Koch C . Theta phase segregation of input-specific gamma patterns in entorhinal-hippocampal networks. Neuron. 2014; 84(2):470-85. PMC: 4253689. DOI: 10.1016/j.neuron.2014.08.051. View

18.

Sheikhattar A, Miran S, Liu J, Fritz J, Shamma S, Kanold P . Extracting neuronal functional network dynamics via adaptive Granger causality analysis. Proc Natl Acad Sci U S A. 2018; 115(17):E3869-E3878. PMC: 5924897. DOI: 10.1073/pnas.1718154115. View

19.

Hoffman K, Dragan M, Leonard T, Micheli C, Montefusco-Siegmund R, Valiante T . Saccades during visual exploration align hippocampal 3-8 Hz rhythms in human and non-human primates. Front Syst Neurosci. 2013; 7:43. PMC: 3757337. DOI: 10.3389/fnsys.2013.00043. View

20.

SCHILLER P, Lee K . The role of the primate extrastriate area V4 in vision. Science. 1991; 251(4998):1251-3. DOI: 10.1126/science.2006413. View