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How the Human Brain Masters Time

Periodic Reporting for period 4 - BiT (How the Human Brain Masters Time)

Reporting period: 2021-04-01 to 2022-09-30

BiT aimed to understand where, how and when the human brain represents and processes time in a range spanning from a few hundreds of milliseconds to a few seconds. Specifically, BiT addressed the following research issues: a) it asked whether duration, similarly to other sensory features, is represented in the brain via duration tuning and topography i.e. neural units selectively responsive to different durations and orderly mapped in contiguous portions of the cortical surface; b) it wondered whether spatial and temporal information are processed within the same neural circuits i.e. are the duration of a visual object and its spatial position processed together? c) it explored the functional role of visual areas in temporal encoding and perception; d) it investigated the functional connectivity and the temporal hierarchies within sensory modality-specific and sensory modality-independent “time regions” i.e. which region is connected to which and which region comes first? To address those goals, BiT used the full palette of human neuroscience techniques: psychophysics, neuroimaging, brain stimulation techniques and the simultaneous combination of the two. By being able to answer these questions, BiT research will have an impact on the field of temporal cognition and on human cognition in general. BiT gained knowledge on how the perception of time is achieved in the adult brain. These findings will prompt further work to investigate brain changes underlying time perception deficits, and to develop new methods for manipulating time perception in healthy and clinical populations.
The goal of BiT was the understanding of the neural mechanisms underlying the perception of time in a range spanning from hundreds of milliseconds to a few seconds. To meet this goal, the entire project was structured in three working packages (WPs).
In WP1 with a series of fMRI experiments at ultra-high field (7T) we tested a new biologically plausible hypothesis of temporal representation via duration tuning and topography. In these studies, we showed the existence in parietal, occipital and frontal cortices of duration preferences, in SMA these preferences were topographically organized. Chronomaps show a high degree of flexibility of representation. They can indeed change according to the duration range and the temporal context hand, the perception, and the association with a different magnitude dimension like numerosity. Duration preferences in SMA and parietal cortex are present for both visual and auditory stimuli.
The aim of WP2 was to better specify the functional role of sensory cortices in time perception and to explore the link between spatial and temporal information within these areas. In a series of TMS experiments we first showed that spatial and temporal information are processed within the same neural circuits in visual cortex and follows the spatial topography. In addition, we showed that the causal engagement of primary visual cortex and extrastriate area V5/MT in time encoding is strongest while the stimulus unfolds over time and depends on the nature i.e. filled versus empty, of the temporal interval at hand. With two EEG experiments we then used perceptual adaptation (to either duration or temporal frequency) to distort stimulus duration perception and we showed that time distortions can be predicted by an early event related component (ERP N200) and an increase in the Beta band frequency spectrum in posterior electrodes contralateral to the adapted stimulus. Overall, our findings suggest that local and low-level perceptual processes are involved in generating a subjective sense of time. In WP3 we assessed the functional relationship and the temporal hierarchies between putative “time regions”. With two TMS and an EEG/TMS experiment we showed the existence of a cortical hierarchy of visual (V1) parietal (IPL) and frontal regions (SMA) associated to a temporal discrimination task, where early ERP component in V1 and SMA are necessary to temporal judgments. Moreover, we showed that while occipital areas are active during the encoding of stimulus duration probably via accumulation of sensory input, SMA is the area that reads-out this signal and has a high-level representation of stimulus duration.
Finally using Dynamic Causal Modelling, we were able to identify the effective connectivity structure between the cerebellum and this cortical network. The results highlight the role of the cerebellum as the network hub and that of SMA as the final stage of duration recognition. Interestingly, when a specific duration is presented, only the communication strength between the units selective to that specific duration and to the neighboring durations is affected. These findings link for the first time, duration preferences within single brain region with connectivity dynamics between regions, suggesting a communication mode that is partially duration specific.
The groundbreaking achievement of BiT comes from its most challenging and novel ideas: the existence of a network of brain areas displaying selective responses to stimulus timing and organized into topographic maps by their timing preferences. This finding shows, for the first time in the human brain, that the adaptive representation of an abstract feature such as time, that lacks a sensory organ, can be achieved by a topographical arrangement of duration-sensitive neural populations similar to that observed in several cortical and subcortical structures for the processing of sensory and motor signals. Demonstrating the existence of chronomaps represents a significant and groundbreaking step forward our understanding of the neural representation of time since it shows a possible mechanism of temporal representation and its location in the brain (what is the mechanism and where it is). This finding will challenge current models of time perception and open up new approaches to the study of time processing and more in general to cognitive neuroscience. From generally looking at brain regions processing time (i.e. a single mechanism, a single neural circuit where all durations are processed similarly and have a similar status), we can move towards the idea of a greater specificity in the processing of different durations (where each duration has a specific status and a specific relationship with others within a map). The effect of this change of approach will have consequences that will go beyond the length of the ERC project. For example, temporal maps (either sensory or read-out) could in future become a neurophysiological marker of the efficiency of temporal mechanisms in the brain. This may be used as diagnostic tool and prompt future research to investigates temporal deficits. This is particularly important since time deficits are common in neurological and psychiatric disorders but also in aging populations, they are highly disruptive of every-day life activities, but they rarely become the target of treatment.
Figure 1 fMRI results, comparison between the chronotopic maps of two experiments