A Network of Topographic Maps in Human Association Cortex Hierarchically Transforms Visual Timing-Selective Responses

Harvey, Ben M.; Dumoulin, Serge O.; Fracasso, Alessio; Paul, Jacob

doi:10.2139/ssrn.3438365

Cited by 5 publications

(5 citation statements)

References 25 publications

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“…Previous studies have pointed to a broad network of neural regions engaged in temporal processing, including the supplementary motor area (SMA), inferior frontal gyrus (IFG), cerebellum and basal ganglia (Wiener et al, 2010b;Hayashi et al, 2014Hayashi et al, , 2018Protopapa et al, 2019;Harvey et al, 2020). Although the ROI approach utilized here was designed to focus on right SMG, it is noteworthy that none of these cortical or subcortical areas showed duration-selective attenuation of the BOLD response in the exploratory, whole brain analysis.…”

Section: Discussionmentioning

confidence: 99%

Duration Selectivity in Right Parietal Cortex Reflects the Subjective Experience of Time

Hayashi

Ivry

2020

J. Neurosci.

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The perception of duration in the subsecond range has been hypothesized to be mediated by the population response of duration-sensitive units, each tuned to a preferred duration. One line of support for this hypothesis comes from neuroimaging studies showing that cortical regions, such as in parietal cortex exhibit duration tuning. It remains unclear if this representation is based on the physical duration of the sensory input or the subjective duration, a question that is important given that our perception of the passage of time is often not veridical, but rather, biased by various contextual factors. Here we used fMRI to examine the neural correlates of subjective time perception in human participants. To manipulate perceived duration while holding physical duration constant, we employed an adaptation method, in which, prior to judging the duration of a test stimulus, the participants were exposed to a train of adapting stimuli of a fixed duration. Behaviorally, this procedure produced a pronounced negative aftereffect: A short adaptor biased participants to judge stimuli as longer and a long adaptor biased participants to judge stimuli as shorter. Duration tuning modulation, manifest as an attenuated BOLD response to stimuli similar in duration to the adaptor, was only observed in the right supramarginal gyrus (SMG) of the parietal lobe and middle occipital gyrus, bilaterally. Across individuals, the magnitude of the behavioral aftereffect was positively correlated with the magnitude of duration tuning modulation in SMG. These results indicate that duration-tuned neural populations in right SMG reflect the subjective experience of time. 3 Significance statement The subjective sense of time is a fundamental dimension of sensory experience. To investigate the neural basis of subjective time, we conducted an fMRI study, using an adaptation procedure that allowed us to manipulate perceived duration while holding physical duration constant. Regions within the occipital cortex and right parietal lobe showed duration tuning that was modulated when the test stimuli were similar in duration to the adaptor. Moreover, the magnitude of the distortion in perceived duration was correlated with the degree of duration tuning modulation in the parietal region. These results provide strong physiological evidence that the population coding of time in the right parietal cortex reflects our subjective experience of time.

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Section: Discussionmentioning

confidence: 99%

Duration Selectivity in Right Parietal Cortex Reflects the Subjective Experience of Time

Hayashi

Ivry

2020

J. Neurosci.

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“…In this view, the processes underlying subjective time have their neural substrates in perceptual and memory systems, not systems specialized for time itself. Other recent studies of time perception (21,23,41,42) have attempted to correlate maps of neural activity with a specific timing-related behavior, responses, or physical elapsed durations. In contrast, we have taken a model-based approach to describe how sensory information arriving in primary sensory areas is transformed into subjective time.…”

Section: Discussionmentioning

confidence: 99%

Trial-by-trial predictions of subjective time from human brain activity

Sherman

Fountas

Seth

et al. 2020

Preprint

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Author ContributionsWR conceived of the study. MTS and WR designed and pre-registered the experiments and analyses. MTS collected, analyzed, and constructed models of human behavioral and neuroimaging data. ZF constructed the artificial network model and analyzed the data. MTS and WR wrote the manuscript. AKS and ZF provided critical revisions on the manuscript. AbstractHuman experience of time exhibits systematic, context-dependent deviations from objective clock time. For example, time is experienced differently at work than on holiday. The cognitive and neural bases of how time perception interacts with the content of experience remain unclear, and leading explanations of human time perception are not equipped to explain this interaction. We propose an alternative account of human time perception, based on the dynamics of sensory processing. Our approach naturally links content of experience with time perception through a common foundation in basic sensory processing. We provide evidence for this proposal in model-based analyses of the dynamics of perceptual processing in an artificial neural network and in the activity of human sensory cortex. Healthy human participants watched naturalistic, silent videos and estimated their duration while fMRI was acquired. The same videos were used as stimuli for the artificial network.We constructed a computational model that predicted video durations from salient events in the activity of the artificial network, or in participants' visual cortex. The artificial network model reproduced human-like duration estimates, including biases in estimation depending on the content of a given video. Most importantly, the model based on human visual cortex activity reproduced trial-by-trial biases in our human participants' subjective reports, whereas control models trained on auditory or somatosensory activity did not. Together, our results reveal that human subjective time is based on information arising during the processing of our dynamic sensory environment, providing a computational basis for an end-to-end account of time perception. Significance StatementOur perception of time depends on the contents of experience, reflected in expressions such as "a watched pot never boils". Prevailing accounts of human time perception cannot provide good explanations for this. We tested a new explanation: time perception arises from the processing of our dynamic sensory environment. Supporting this theory, human participants' duration reports of silent videos correlated with estimates we reconstructed from activity in the visual cortex of their brain while they watched those videos. This was not a brain-wide phenomenon; reconstructions based on other brain regions did not correlate with subjective reports of duration. Our results validate our new theory, linking content of experience and perception of time through a common foundation in basic sensory processing.

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“…Interestingly, recent evidence revealed a clear gradient organization along the anterior-posterior axis of SMA, with anterior and posterior SMA sub-regions showing preferential activations for short and long durations, respectively (Protopapa et al, 2019; see also Harvey et al, 2019). This durationsensitive tuning organized in a gradient might be a good candidate to sequentially integrate temporal pulses into a representation of durations.…”

Section: Common Neural Network For Space and Timementioning

confidence: 93%

“…For example, a study showed that, similar to visual cortex, human fronto-parietal cortices contain topographic representations of eccentricity and polar angle, which are organized into clusters so that to represent all the gradients of polar angle of the contralateral visual field (Mackey, Winawer, & Curtis, 2017). Likewise, very recent evidence identified topographic timing maps or chronotopic maps in several brain regions, including not only sensory cortices but also frontal, parietal areas and SMA (Harvey, Damoulin, Fracasso, & Paul, 2019;Protopapa et al, 2019).…”

Section: 'Gradiatom': Functional Gradients Underlying Space and Timementioning

confidence: 99%

FromATOMtoGradiATOM: Cortical gradients support time and space processing as revealed by a meta-analysis of neuroimaging studies

Cona

Wiener

Scarpazza

2020

Preprint

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According to the ATOM (A Theory Of Magnitude), formulated by Walsh more than fifteen years ago, there is a general system of magnitude in the brain that comprises regions, such as the parietal cortex, shared by space, time and other magnitudes (Walsh, 2003).The present meta-analysis of neuroimaging studies used the Activation Likelihood Estimation (ALE) method in order to determine the set of regions commonly activated in space and time processing and to establish the neural activations specific to each magnitude domain. Following PRISMA guidelines, we included in the analysis a total of 112 and 114 experiments, exploring space and time processing, respectively.We clearly identified the presence of a system of brain regions commonly recruited in both space and time and that includes: bilateral insula, the pre-supplementary motor area (SMA), the right frontal operculum and the intraparietal sulci. These regions might be the best candidates to form the core magnitude neural system. Surprisingly, along each of these regions but the insula, ALE values progressed in a cortical gradient from time to space. The SMA exhibited an anterior-posterior gradient, with space activating more-anterior regions (i.e., pre-SMA) and time activating moreposterior regions (i.e., SMA-proper). Frontal and parietal regions showed a dorsal-ventral gradient: space is mediated by dorsal frontal and parietal regions, and time recruits ventral frontal and parietal regions.Our study supports but also expands the ATOM theory. Therefore, we here re-named it the 'GradiATOM' theory (Gradient Theory of Magnitude), proposing that gradient organization can facilitate the transformations and integrations of magnitude representations by allowing space-and time-related neural populations to interact with each other over minimal distances.

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A Network of Topographic Maps in Human Association Cortex Hierarchically Transforms Visual Timing-Selective Responses

Cited by 5 publications

References 25 publications

Duration Selectivity in Right Parietal Cortex Reflects the Subjective Experience of Time

Duration Selectivity in Right Parietal Cortex Reflects the Subjective Experience of Time

Trial-by-trial predictions of subjective time from human brain activity

FromATOMtoGradiATOM: Cortical gradients support time and space processing as revealed by a meta-analysis of neuroimaging studies

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