Individuals time as if using a stopwatch that can be stopped or reset on command. Here, we review behavioural and neurobiological data supporting the time-sharing hypothesis that perceived time depends on the attentional and memory resources allocated to the timing process. Neuroimaging studies in humans suggest that timekeeping tasks engage brain circuits typically involved in attention and working memory. Behavioural, pharmacological, lesion and electrophysiological studies in lower animals support this time-sharing hypothesis. When subjects attend to a second task, or when intruder events are presented, estimated durations are shorter, presumably due to resources being taken away from timing. Here, we extend the time-sharing hypothesis by proposing that resource reallocation is proportional to the perceived contrast, both in temporal and non-temporal features, between intruders and the timed events. New findings support this extension by showing that the effect of an intruder event is dependent on the relative duration of the intruder to the intertrial interval. The conclusion is that the brain circuits engaged by timekeeping comprise not only those primarily involved in time accumulation, but also those involved in the maintenance of attentional and memory resources for timing, and in the monitoring and reallocation of those resources among tasks.
BACKGROUND: Current theories of interval timing assume that humans and other animals time as if using a single, absolute stopwatch that can be stopped or reset on command. Here we evaluate the alternative view that psychological time is represented by multiple clocks, and that these clocks create separate temporal contexts by which duration is judged in a relative manner. Two predictions of the multiple-clock hypothesis were tested. First, that the multiple clocks can be manipulated (stopped and/or reset) independently. Second, that an event of a given physical duration would be perceived as having different durations in different temporal contexts, i.e., would be judged differently by each clock. METHODOLOGY/PRINCIPAL FINDINGS: Rats were trained to time three durations (e.g., 10, 30, and 90 s). When timing was interrupted by an unexpected gap in the signal, rats reset the clock used to time the "short" duration, stopped the "medium" duration clock, and continued to run the "long" duration clock. When the duration of the gap was manipulated, the rats reset these clocks in a hierarchical order, first the "short", then the "medium", and finally the "long" clock. Quantitative modeling assuming re-allocation of cognitive resources in proportion to the relative duration of the gap to the multiple, simultaneously timed event durations was used to account for the results. CONCLUSIONS/SIGNIFICANCE: These results indicate that the three event durations were effectively timed by separate clocks operated independently, and that the same gap duration was judged relative to these three temporal contexts. Results suggest that the brain processes the duration of an event in a manner similar to Einstein's special relativity theory: A given time interval is registered differently by independent clocks dependent upon the context.
In two experiments, the peak-interval procedure was used with humans to test effects related to gaps in multisecond timing. In Experiment 1, peak times of response distributions were shorter when the gap occurred later during the encoding of the criterion time to be reproduced, suggesting that gap expectancy shortened perceived durations. Peak times were also positively related to objective target durations. Spreads of response distributions were generally related to estimated durations. In Experiment 2, peak times were shortest when gaps were expected but did not occur, confirming that the shortening effect of gap expectancy is independent of the gap occurrence. High positive start-stop correlations and moderate positive peak-time-spread correlations showed strong memory variability, whereas low and negative start-spread correlations suggest small response-threshold variability. Correlations seemed not to be influenced by expectancy. Overall, the peak-interval procedure with gaps provided relevant information on similarities and differences in timing in humans and other animals.
Much remains to be understood about the differential contributions from primary and secondary sensory cortices to sensory-guided decision making. To address this issue we simultaneously recorded activity from neuronal ensembles in primary [gustatory cortex GC)] and secondary gustatory [orbitofrontal cortex (OFC)] cortices while rats made a taste-guided decision between two response alternatives. We found that before animals commenced a response guided by a tastant cue, GC ensembles contained more information than OFC about the response alternative about to be selected. Thereafter, while the animal's response was underway, the response-selective information in ensembles from both regions increased, albeit to a greater degree in OFC. In GC, this increase depends on a representation of the taste cue guiding the animal's response. The increase in the OFC also depends on the taste cue guiding and other features of the response such as its spatiomotor properties and the behavioral context under which it is executed. Each of these latter features is encoded by different ensembles of OFC neurons that are recruited at specific times throughout the response selection process. These results indicate that during a taste-guided decision task both primary and secondary gustatory cortices dynamically encode different types of information.
Behavioral studies have demonstrated that time perception in adults, children, and nonhuman animals is subject to Weber's Law. More specifically, as with discriminations of other features, it has been found that it is the ratio between two durations rather than their absolute difference that controls the ability of an animal to discriminate them. Here, we show that scalp-recorded event-related electrical brain potentials (ERPs) in both adults and 10-month-old human infants, in response to changes in interstimulus interval (ISI), appear to obey the scalar property found in time perception in adults, children, and nonhuman animals. Using a timing-interval oddball paradigm, we tested adults and infants in conditions where the ratio between the standard and deviant interval in a train of homogeneous auditory stimuli varied such that there was a 1:4 (only for the infants), 1:3, 1:2, and 2:3 ratio between the standard and deviant intervals. We found that the amplitude of the deviant-triggered mismatch negativity ERP component (deviant-ISI ERP minus standard-ISI ERP) varied as a function of the ratio of the standard to deviant interval. Moreover, when absolute values were varied and ratio was held constant, the mismatch negativity did not vary.
Choline supplementation of the maternal diet has long-term facilitative effects on spatial and temporal memory processes in the offspring. To further delineate the impact of early nutritional status on brain and behavior, we examined effects of prenatal-choline availability on hippocampal oscillatory frequency bands in 12 month-old male and female rats. Adult offspring of time-pregnant dams that were given a deficient level of choline (DEF=0.0 g/kg), sufficient choline (CON=1.1 g/kg) or supplemental choline (SUP=3.5 g/kg) in their chow during embryonic days (ED) 12-17 were implanted with an electroencephalograph (EEG) electrode in the hippocampal dentate gyrus in combination with an electromyograph (EMG) electrode patch implanted in the nuchal muscle. Five consecutive 8-h recording sessions revealed differential patterns of EEG activity as a function of awake, slow-wave sleep (SWS) and rapid-eye movement (REM) sleep states and prenatal choline status. The main finding was that SUP rats displayed increased power levels of gamma (30-100 Hz) band oscillations during all phases of the sleep/wake cycle. These findings are discussed within the context of a general review of neuronal oscillations (e.g., delta, theta, and gamma bands) and synchronization across multiple brain regions in relation to sleep-dependent memory consolidation in the hippocampus.
Interval timing in the seconds-to-minutes range is crucial to learning, memory, and decision-making. Recent findings argue for the involvement of cortico-striatal circuits that are optimized by the dopaminergic modulation of oscillatory activity and lateral connectivity at the level of cortico-striatal inputs. Striatal medium spiny neurons are proposed to detect the coincident activity of specific beat patterns of cortical oscillations, thereby permitting the discrimination of supra-second durations based upon the reoccurring patterns of subsecond neural firing. This proposal for the cortico-striatal representation of time is consistent with the observed psychophysical properties of interval timing (e.g. linear time scale and scalar variance) as well as much of the available pharmacological, lesion, patient, electrophysiological, and neuroimaging data from animals and humans (e.g. dopamine-related timing deficits in Huntington's and Parkinson's disease as well as related animal models). The conclusion is that although the striatum serves as a 'core timer', it is part of a distributed timing system involving the coordination of large-scale oscillatory networks.
In order to determine brain and behavioral sensitivity of nutrients that may serve as inductive signals during early development, we altered choline availability to rats during 7 time frames spanning embryonic day (ED) 6 through postnatal day (PD) 75 and examined spatial memory ability in the perinatally-treated adults. Two sensitive periods were identified, ED 12-17 and PD 16-30, during which choline supplementation facilitated spatial memory and produced increases in dendritic spine density in CA1 and dentate gyrus (DG) regions of the hippocampus while also changing the dendritic fields of DG granule cells. Moreover, choline supplementation during ED 12-17 only, prevented the memory decline normally observed in aged rats. These behavioral changes were strongly correlated with the acetylcholine (ACh) content of hippocampal slices following stimulated release. Our data demonstrate that the availability of choline during critical periods of brain development influences cognitive performance in adulthood and old age, and emphasize the importance of perinatal nutrition for successful cognitive aging.
A fundamental assumption underlying research in translational neuroscience is that animal models represent many of the same neurocognitive mechanisms and decision processes used by humans. Clear demonstrations of such correspondences will be crucial to the discovery of the neurobiological underpinnings of higher-level cognition. One domain likely to support fruitful comparisons is interval timing, because humans and other animals appear to share basic similarities in their ability to discriminate the durations of events in the seconds-to-minutes range. Here, we report that in a duration-bisection procedure using a series of anchor durations ranging from 2 through 5 s, pigeon, mouse, and human subjects classified a given signal duration as subjectively shorter than an adjacent, physically shorter signal duration when the two durations lay on opposite sides of a putative category boundary. These bisection reversals provide strong evidence for continuity of temporal cognition across a wide range of vertebrate species.
Our sense of time is altered by our emotions to such an extent that time seems to fly when we are having fun and drags when we are bored. Recent studies using standardized emotional material provide a unique opportunity for understanding the neurocognitive mechanisms that underlie the effects of emotion on timing and time perception in the milliseconds-to-hours range. We outline how these new findings can be explained within the framework of internal-clock models and describe how emotional arousal and valence interact to produce both increases and decreases in attentional time sharing and clock speed. The study of time and emotion is at a crossroads, and we outline possible examples for future directions.
Time is a fundamental dimension of life. It is crucial for decisions about quantity, speed of movement and rate of return, as well as for motor control in walking, speech, playing or appreciating music, and participating in sports. Traditionally, the way in which time is perceived, represented and estimated has been explained using a pacemaker-accumulator model that is not only straightforward, but also surprisingly powerful in explaining behavioural and biological data. However, recent advances have challenged this traditional view. It is now proposed that the brain represents time in a distributed manner and tells the time by detecting the coincidental activation of different neural populations.