Gamma oscillations in the superior colliculus and pulvinar in response to faces support discrimination performance in monkeys

Le, Quan Van; Nishimaru, Hiroshi; Matsumoto, Jumpei; Takamura, Yusaku; Nguyen, Manh Duc; Mao, Can Van; Hori, Etsuro; Maior, Rafael S.; Tomaz, Carlos; Ono, Taketoshi; Nishijo, Hisao

doi:10.1016/j.neuropsychologia.2017.10.015

Cited by 14 publications

(12 citation statements)

References 83 publications

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“…Previous experimental studies have shown that neuronal populations of the pulvinar nucleus possess multiple dynamic activity profiles [Wrobel et al, 2007, Saalmann and Kastner, 2011, Yu et al, 2018, Le et al, 2019. In this work, using a theoretical approach, we propose that such population dynamics in the pulvinar may arise from cortico-thalamic connections originating from different hierarchical cortical areas, whose axonal terminals have distinct anatomical and physiological profiles.…”

Section: Discussionmentioning

confidence: 88%

Corticothalamic Projections Gate Alpha Rhythms in the Pulvinar

Cortes

Farishta

Ladret

et al. 2021

Preprint

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Two types of corticothalamic (CT) terminals reach the pulvinar nucleus of the thalamus, and their distribution varies according to the hierarchical level of the cortical area they originate from. While type 2 terminals are more abundant at lower hierarchical levels, terminals from higher cortical areas mostly exhibit type 1 axons. Such terminals also evoke different excitatory postsynaptic potential dynamic profiles, presenting facilitation for type 1 and depression for type 2. As the pulvinar is involved in the oscillatory regulation between intercortical areas, fundamental questions about the role of these different terminal types in the neuronal communication throughout the cortical hierarchy are yielded. Our theoretical results support that the co-action of the two types of terminals produces different oscillatory rhythms in pulvinar neurons. More precisely, terminal types 1 and 2 produce alpha-band oscillations at a specific range of connectivity weights. Such oscillatory activity is generated by an unstable transition of the balanced state network's properties that it is found between the quiescent state and the stable asynchronous spike response state. While CT projections from areas 17 and 21a are arranged in the model as the empirical proportion of terminals types 1 and 2, the actions of these two cortical connections are antagonistic. As area 17 generates low-band oscillatory activity, cortical area 21a shifts pulvinar responses to stable asynchronous spiking activity and vice-versa when area 17 produces an asynchronous state. To further investigate such oscillatory effects through corticothalamo-cortical projections, the transthalamic pathway, we created a cortical feedforward network of two cortical areas, 17 and 21a, with CT connections to a pulvinar-like network. With this model, the transthalamic pathway propagates alpha waves from the pulvinar to area 21a. This oscillatory transfer ceases when reciprocal connections from area 21a reach the pulvinar, closing the cortico-thalamic loop. Taken together, results of our model suggest that the pulvnar shows a bi-stable spiking activity, oscillatory or regular asynchronous spiking, whose responses are gated by the different activation of cortico-pulvinar projections from lower to higher-order areas such as areas 17 and 21a.

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Section: Discussionmentioning

confidence: 88%

Corticothalamic Projections Gate Alpha Rhythms in the Pulvinar

Cortes

Farishta

Ladret

et al. 2021

Preprint

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“…Thus, it seems likely that the origin of stimulus-phase-locked oscillations is an effect of two phenomena, intrinsic neuronal properties and local network connections involving GABA-ergic neurons. Induced stimulus-phase-locked oscillations are not unique to the SC and were also found in the spiking (Gray and Singer, 1989; Gray et al, 1989; Bringuier et al, 1997; Friedman-Hill et al, 2000; Womelsdorf et al, 2012; Baranauskas et al, 2016; Le et al, 2017) or EEG activity (Tallon-Baudry et al, 1996) of the visual and auditory cortices (Noda et al, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…There are a limited number of publications concerning the presence of oscillations and/or oscillatory synchronization of neuronal activity in the optic tectum (cat SC: Mandl, 1993; Brecht et al, 1998, 1999, 2001; birds: Neuenschwander et al, 1999; Chabli et al, 2000; Goddard et al, 2012; ferret: Stitt et al, 2013; rat: Baranauskas et al, 2016; monkey: Le et al, 2017). Moreover, these reports are somewhat inconclusive, in that some data showed oscillations in the SC that were dependent on stimulus velocity (Mandl, 1993; Chabli et al, 2000; Pauluis et al, 2001), while other data showed a lack of dependency on stimulus velocity (Brecht et al, 1998, 2001).…”

Section: Introductionmentioning

confidence: 99%

Oscillations in Spontaneous and Visually Evoked Neuronal Activity in the Superficial Layers of the Cat's Superior Colliculus

Foik

Ghazaryan

Waleszczyk

2018

Front. Syst. Neurosci.

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Oscillations are ubiquitous features of neuronal activity in sensory systems and are considered as a substrate for the integration of sensory information. Several studies have described oscillatory activity in the geniculate visual pathway, but little is known about this phenomenon in the extrageniculate visual pathway. We describe oscillations in evoked and background activity in the cat's superficial layers of the superior colliculus, a retinorecipient structure in the extrageniculate visual pathway. Extracellular single-unit activity was recorded during periods with and without visual stimulation under isoflurane anesthesia in the mixture of N2O/O2. Autocorrelation, FFT and renewal density analyses were used to detect and characterize oscillations in the neuronal activity. Oscillations were common in the background and stimulus-evoked activity. Frequency range of background oscillations spanned between 5 and 90 Hz. Oscillations in evoked activity were observed in about half of the cells and could appear in two forms —stimulus-phase-locked (10–100 Hz), and stimulus-phase-independent (8–100 Hz) oscillations. Stimulus-phase-independent and background oscillatory frequencies were very similar within activity of particular neurons suggesting that stimulus-phase-independent oscillations may be a form of enhanced “spontaneous” oscillations. Stimulus-phase-locked oscillations were present in responses to moving and flashing stimuli. In contrast to stimulus-phase-independent oscillations, the strength of stimulus-phase-locked oscillations was positively correlated with stimulus velocity and neuronal firing rate. Our results suggest that in the superficial layers of the superior colliculus stimulus-phase-independent oscillations may be generated by the same mechanism(s) that lie in the base of “spontaneous” oscillations, while stimulus-phase-locked oscillations may result from interactions within the intra-collicular network and/or from a phase reset of oscillations present in the background activity.

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“…Thus, it seems likely that the origin of stimulus-phase-locked oscillations is an effect of two phenomena, intrinsic neuronal properties and local network connections involving GABA-ergic neurons. Induced stimulus-phase-locked oscillations are not unique to the SC and were also found in the spiking Bringuier et al 1997;Friedman-Hill et al 2000;Womelsdorf et al 2012;Baranauskas et al 2016;Le et al 2017) or EEG activity (Tallon-Baundry et al 1996) of the visual and auditory cortices (Noda et al 2013).…”

Section: Origin Of Stimulus-phase-locked Oscillations In the Sscmentioning

confidence: 99%

Oscillations in spontaneous and visually evoked neuronal activity in the superficial layers of the cat’s superior colliculus

Foik

Ghazaryan

Waleszczyk

2018

Preprint

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Number of words for Abstract: 262 Number of words for Introduction: 660Number of words for Manuscript: 8261 AbstractOscillations are ubiquitous features of neuronal activity in sensory systems and are considered as a substrate for the integration of sensory information. Several studies have described oscillatory activity in the geniculate visual pathway, but little is known about this phenomenon in the extrageniculate visual pathway. We describe oscillations in evoked and background activity in the cat's superficial layers of the superior colliculus, a retinorecipient structure in the extrageniculate visual pathway. Extracellular singleunit activity was recorded during periods with and without visual stimulation under isoflurane anesthesia in the mixture of N 2 O/O 2 . Autocorrelation, FFT and renewal density analyses were used to detect and characterize oscillations in the neuronal activity. Oscillations were common in the background and stimulus-evoked activity.Frequency range of background oscillations spanned between 5 -90 Hz. Oscillations in evoked activity were observed in about half of the cells and could appear in two formsstimulus-phase-locked (10 -100 Hz), and stimulus-phase-independent (8 -100 Hz) oscillations. Stimulus-phase-independent and background oscillatory frequencies were very similar within activity of particular neurons suggesting that stimulus-phaseindependent oscillations may be a form of enhanced "spontaneous" oscillations.Stimulus-phase-locked oscillations were present in responses to moving and flashing stimuli. In contrast to stimulus-phase-independent oscillations, the strength of stimulusphase-locked oscillations was positively correlated with stimulus velocity and neuronal firing rate. Our results suggest that in the superficial layers of the superior colliculus stimulus-phase-independent oscillations may be generated by the same mechanism(s) that lie in the base of "spontaneous" oscillations, while stimulus-phase-locked oscillations may result from interactions within the intra-collicular network and/or from a phase reset of oscillations present in the background activity.Abbreviations ACH, autocorrelation histogram; cACH, corrected autocorrelation histogram; DiI, 1,1'dioctadecyl-3.3,3',3'-tetramethylindocarbocyanine perchlorate: ECoG, electrocorticogram; FFT, Fast Fourier Transform; ISI, interspike interval histogram;LGN, lateral geniculate nucleus; PSTH, peri-stimulus time histogram; r, Pearson correlation coefficient; rACH, raw autocorrelation histogram; RDA, renewal density analysis; RF, receptive field; SC, superior colliculus; sSC, superficial layers of superior colliculus; std(FFT), standard deviation of power spectrum;

show abstract

Gamma oscillations in the superior colliculus and pulvinar in response to faces support discrimination performance in monkeys

Cited by 14 publications

References 83 publications

Corticothalamic Projections Gate Alpha Rhythms in the Pulvinar

Corticothalamic Projections Gate Alpha Rhythms in the Pulvinar

Oscillations in Spontaneous and Visually Evoked Neuronal Activity in the Superficial Layers of the Cat's Superior Colliculus

Oscillations in spontaneous and visually evoked neuronal activity in the superficial layers of the cat’s superior colliculus

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