Visual cortex encodes timing information in humans and mice

Yu, Qingpeng; Bi, Zedong; Jiang, Shize; Yan, Biao; Chen, Heming; Wang, Yiting; Miao, Yizhan; Li, Kexin; Wei, Zixuan; Xie, Yuanting; Tan, Xinrong; Fu, Hang; Cui, Lianxian; Lü, Xing; Weng, Shi-Jun; Wang, Xin; Yuan, Yuanzhi; Zhou, Changsong; Wang, Gang; Li, Liang; Ma, Li; Mao, Ying; Chen, Liang; Zhang, Jiayi

doi:10.1016/j.neuron.2022.09.008

Cited by 8 publications

(7 citation statements)

References 76 publications

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“…Based on previous studies, we hypothesized that attention modulates the different features in distinct ways, which means the modulation to different features would happen on different frequency bands and time ranges. For the frequency bands, we hypothesize that the delta band reflects attentional modulation of the semantic feature( Dai et al, 2022; Teoh et al, 2022; Yu et al, 2022 ), and the theta band represents the acoustic feature( Ding et al, 2014; Etard et al, 2019 ). The entrainment to the speaker’s neural feature needs further exploration.…”

Section: Introductionmentioning

confidence: 99%

EEG-based speaker-listener neural coupling reflects speech-selective attentional mechanisms beyond the speech stimulus

Hong

Nolte

et al. 2022

Preprint

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When we are following someone when there are multiple speakers, are we just paying attention to the sound the speaker makes, the word the speaker uses, or are we aligning our minds to the attended speaker? In this process, selective attention plays a critical role. Previous studies have mainly focused on attention modulation on the single types of features from the speaker. However, attending to a speaker needs an integrative process: the sound waves, which represent acoustic features, should be heard; the meaning of the text, which represents semantic features, needs to be understood; listeners and speakers need to form a common grounding during the process, which represent the inter-brain feature. We still do not know how our brain entrains different types of features from the speaker in an integrative way. In this study, naturalistic speech was adopted to explore attention modulation. The natural language processing models and the flourishing inter-brain recording methods were adopted to qualify the different types of information from the speaker. Our study revealed that attention modulated the acoustic, semantic, and speaker's neural activity in an integrative way. When the listener pays attention to a speaker, the sound is the first to be processed: The neural activity in the theta band entrains the acoustic feature with a latency of 200~350 ms. Then, the meaning of the attended speech is parsed: the delta band modulates the attention with a latency of 200~600 ms. The listener entrains the speaker's neural activity 5 seconds before the speech onset. The entrainment of the acoustic feature and the semantic feature is correlated with each other. Only the entrainment of the attended speaker has a significant negative correlation with the comprehension score. Together, these results illustrate an integrative view of how our brain is selectively entrained to different types of information from the speaker.

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Section: Introductionmentioning

confidence: 99%

EEG-based speaker-listener neural coupling reflects speech-selective attentional mechanisms beyond the speech stimulus

Hong

Nolte

et al. 2022

Preprint

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“…Spatiotemporal prediction has also been found in V1 in mice performing foraging tasks in virtual reality (Fiser et al, 2016;Yu et al, 2022). Nevertheless, these findings did not explicitly test temporal processing in a sensory discrimination task, and an outstanding question was how temporal information was computationally encoded in V1.…”

Section: Discussionmentioning

confidence: 97%

Temporal information of subsecond sensory stimuli in primary visual cortex is encoded via high dimensional population vectors

Post,

Mol,

Rahmatullah

et al. 2024

Preprint

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Whether in music, language, baking, or memory, our experience of the world is fundamentally linked to time. However, it is unclear how temporal information is encoded, particularly in the range of milliseconds to seconds. Temporal processing at this scale is critical to prediction and survival, such as in a prey anticipating not only where a charging predator will go but alsowhenthe predator will arrive at that location. Several models of timing have been proposed that suggest that either time is encoded intrinsically in the dynamics of a network or that time is encoded by mechanisms that are explicitly dedicated to temporal processing. To determine how temporal information is encoded, we recorded neural activity in primary visual cortex (V1) as mice (male and female) performed a goal directed sensory discrimination task, in which patterns of subsecond stimuli differed only in their temporal profiles. We found that temporal information was encoded in the changing population vector of the network and that the space between these vectors was maximized in learned sessions. Our results suggest that temporal information in the subsecond range is encoded intrinsically and does not rely upon specialized timing mechanisms.SIGNIFICANCE STATEMENTOur experience of the world is fundamentally linked to time, but it is unclear how temporal information is encoded, particularly in the range of milliseconds to seconds. Using a sensory discrimination task in which patterns of subsecond stimuli differed in their temporal profiles, we found that primary visual cortex encodes temporal information via the changing population vector of the network. As temporal processing via population encoding has been shown to rely on inhibitory activity in computational models, our results may provide insight into temporal processing deficits in disorders such as autism spectrum disorder in which there is inhibitory-excitatory imbalance. Furthermore, our results may underlie processing of higher-order sensory stimuli, such as language, that are characterized by complex temporal sequences.

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“…In our task, the duration of time intervals (metronome’s tempos) was defined by a change in the spatial location of a visual stimulus. It is well known from the human psychophysics literature that timing and spatial processing are closely related functions ( 52 – 55 ) that can interfere with each other ( 56 – 59 ) and that might share a common neuronal processing circuitry involving the parietal cortex ( 60 ). In future experiments, we could further explore this space-time relationship ( 61 ) by randomly varying the eccentricity of the response targets, as there is evidence indicating that the eccentricity of a visual stimulus influences its perceived duration ( 62 ).…”

Section: Discussionmentioning

confidence: 99%

Keeping time and rhythm by internal simulation of sensory stimuli and behavioral actions

de Lafuente,

Jazayeri,

Merchant

et al. 2024

Sci. Adv.

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Effective behavior often requires synchronizing our actions with changes in the environment. Rhythmic changes in the environment are easy to predict, and we can readily time our actions to them. Yet, how the brain encodes and maintains rhythms is not known. Here, we trained primates to internally maintain rhythms of different tempos and performed large-scale recordings of neuronal activity across the sensory-motor hierarchy. Results show that maintaining rhythms engages multiple brain areas, including visual, parietal, premotor, prefrontal, and hippocampal regions. Each recorded area displayed oscillations in firing rates and oscillations in broadband local field potential power that reflected the temporal and spatial characteristics of an internal metronome, which flexibly encoded fast, medium, and slow tempos. The presence of widespread metronome-related activity, in the absence of stimuli and motor activity, suggests that internal simulation of stimuli and actions underlies timekeeping and rhythm maintenance.

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Visual cortex encodes timing information in humans and mice

Cited by 8 publications

References 76 publications

EEG-based speaker-listener neural coupling reflects speech-selective attentional mechanisms beyond the speech stimulus

EEG-based speaker-listener neural coupling reflects speech-selective attentional mechanisms beyond the speech stimulus

Temporal information of subsecond sensory stimuli in primary visual cortex is encoded via high dimensional population vectors

Keeping time and rhythm by internal simulation of sensory stimuli and behavioral actions

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