Dissociating explicit timing from temporal expectation with fMRI

Explicit timing is engaged whenever subjects make a deliberate estimate of discrete duration in order to compare it with a previously memorised standard. Conversely, implicit timing is engaged, even without a specific instruction to time, whenever sensorimotor information is temporally structured and can be used to predict the duration of future events. Both emergent timing (motor) and temporal expectation (perceptual) are forms of implicit timing. Recent fMRI studies demonstrate discrete neural substrates for explicit and implicit timing. Specifically, basal ganglia are activated almost invariably by explicit timing, with co-activation of prefrontal, premotor and cerebellar areas being more context-dependent. Conversely, implicit perceptual timing (or "temporal expectation") recruits cortical action circuits, comprising inferior parietal and premotor areas, highlighting its role in the optimisation of prospective behaviour.     

Implicit, predictive timing draws upon the same scalar representation of time as explicit timing

It is not yet known whether the scalar properties of explicit timing are also displayed by more implicit, predictive forms of timing. We investigated whether performance in both explicit and predictive timing tasks conformed to the two psychophysical properties of scalar timing: the Psychophysical law and Weber's law. Our explicit temporal generalization task required overt estimation of the duration of an empty interval bounded by visual markers, whereas our temporal expectancy task presented visual stimuli at temporally predictable intervals, which facilitated motor preparation thus speeding target detection. The Psychophysical Law and Weber's Law were modeled, respectively, by (1) the functional dependence between mean subjective time and real time (2) the linearity of the relationship between timing variability and duration. Results showed that performance for predictive, as well as explicit, timing conformed to both psychophysical properties of interval timing. Both tasks showed the same linear relationship between subjective and real time, demonstrating that the same representational mechanism is engaged whether it is transferred into an overt estimate of duration or used to optimise sensorimotor behavior. Moreover, variability increased with increasing duration during both tasks, consistent with a scalar representation of time in both predictive and explicit timing. However, timing variability was greater during predictive timing, at least for durations greater than 200 msec, and ascribable to temporal, rather than non-temporal, mechanisms engaged by the task. These results suggest that although the same internal representation of time was used in both tasks, its external manifestation varied as a function of temporal task goals.     

An ERP study of temporal discrimination in rats

In this study, we examined event-related potentials (ERPs) in rats performing a timing task. The ERPs were recorded during a timing task and a control task from five regions (frontal cortex, striatum, hippocampus, thalamus, and cerebellum) that are related to time perception. In the timing task, the rats were required to judge the interval between two tones. This interval could be either 500 or 2000 ms. In the control task, only the 500 ms interval between tones was presented and only one lever was available for responses. Any difference in ERPs between the two tasks was considered to reflect the processes that are related to temporal discrimination. The frontal cortex, striatum, and thalamus yielded concurrent differences in ERPs between the two tasks. The results suggest that these regions might play an important role in temporal discrimination.     

The representation of time for motor learning

We have identified factors that control precise motor timing by studying learning in smooth pursuit eye movements. Monkeys tracked a target that moved horizontally for a fixed time interval before changing direction through the addition of a vertical component of motion. After repeated presentations of the same target trajectory, infrequent probe trials of purely horizontal target motion evoked a vertical eye movement around the time when the change in target direction would have occurred. The pursuit system timed the vertical eye movement by keeping track of the duration of horizontal target motion and by measuring the distance the target traveled before changing direction, but not by learning the position in space where the target changed direction. We conclude that high temporal precision in motor output relies on multiple signals whose contributions to timing vary according to task requirements.     

Impaired Temporal Processing of Tactile and Proprioceptive Stimuli in Cerebellar Degeneration

Performance of timed motor sequences relies on the cerebellum and basal ganglia, which integrate proprioceptive information during the motor task and set internal timing mechanisms. Accordingly, these structures are also involved in other temporal processes, such as the discrimination of the different afferent information in the domain of time. In the present study we tested temporal processing of proprioceptive and tactile stimuli in 20 patients with neurodegenerative cerebellar ataxia and 20 age- and sex-matched healthy subjects. Tactile temporal discrimination threshold was defined as the value at which subjects recognized the two stimuli as asynchronous. Temporal discrimination movement threshold of the first dorsal interosseous and flexor carpi radialis was defined as the shortest interval between two paired electrical stimuli in which the subjects blindfolded perceived two separate index finger abductions and wrist flexions. Both tactile and movement temporal discrimination thresholds were higher in patients with cerebellar ataxia. No correlation was found with disease duration and severity. Our study demonstrates that temporal processing of tactile and proprioceptive stimuli is impaired in patients with cerebellar neurodegeneration and highlights the involvement of cerebellum in temporal processing of somatosensory stimuli of different type.     

Influence of the interstimulus interval on temporal processing and learning: testing the state-dependent network model

The ability to determine the interval and duration of sensory events is fundamental to most forms of sensory processing, including speech and music perception. Recent experimental data support the notion that different mechanisms underlie temporal processing in the subsecond and suprasecond range. Here, we examine the predictions of one class of subsecond timing models: state-dependent networks. We establish that the interval between the comparison and the test interval, interstimulus interval (ISI), in a two-interval forced-choice discrimination task, alters the accuracy of interval discrimination but not the point of subjective equality—i.e. while timing was impaired, subjective time contraction or expansion was not observed. We also examined whether the deficit in temporal processing produced by short ISIs can be reduced by learning, and determined the generalization patterns. These results show that training subjects on a task using a short or long ISI produces dramatically different generalization patterns, suggesting different forms of perceptual learning are being engaged. Together, our results are consistent with the notion that timing in the range of hundreds of milliseconds is local as opposed to centralized, and that rapid stimulus presentation rates impair temporal discrimination. This interference is, however, decreased if the stimuli are presented to different sensory channels.     

Motor Activity Improves Temporal Expectancy

Certain brain areas involved in interval timing are also important in motor activity. This raises the possibility that motor activity might influence interval timing. To test this hypothesis, we assessed interval timing in healthy adults following different types of training. The pre- and post-training tasks consisted of a button press in response to the presentation of a rhythmic visual stimulus. Alterations in temporal expectancy were evaluated by measuring response times. Training consisted of responding to the visual presentation of regularly appearing stimuli by either: (1) pointing with a whole-body movement, (2) pointing only with the arm, (3) imagining pointing with a whole-body movement, (4) simply watching the stimulus presentation, (5) pointing with a whole-body movement in response to a target that appeared at irregular intervals (6) reading a newspaper. Participants performing a motor activity in response to the regular target showed significant improvements in judgment times compared to individuals with no associated motor activity. Individuals who only imagined pointing with a whole-body movement also showed significant improvements. No improvements were observed in the group that trained with a motor response to an irregular stimulus, hence eliminating the explanation that the improved temporal expectations of the other motor training groups was purely due to an improved motor capacity to press the response button. All groups performed a secondary task equally well, hence indicating that our results could not simply be attributed to differences in attention between the groups. Our results show that motor activity, even when it does not play a causal or corrective role, can lead to improved interval timing judgments.     

The context of temporal processing is represented in the multidimensional relationships between timing tasks

In the present study we determined the performance interrelations of ten different tasks that involved the processing of temporal intervals in the subsecond range, using multidimensional analyses. Twenty human subjects executed the following explicit timing tasks: interval categorization and discrimination (perceptual tasks), and single and multiple interval tapping (production tasks). In addition, the subjects performed a continuous circle-drawing task that has been considered an implicit timing paradigm, since time is an emergent property of the produced spatial trajectory. All tasks could be also classified as single or multiple interval paradigms. Auditory or visual markers were used to define the intervals. Performance variability, a measure that reflects the temporal and non-temporal processes for each task, was used to construct a dissimilarity matrix that quantifies the distances between pairs of tasks. Hierarchical clustering and multidimensional scaling were carried out on the dissimilarity matrix, and the results showed a prominent segregation of explicit and implicit timing tasks, and a clear grouping between single and multiple interval paradigms. In contrast, other variables such as the marker modality were not as crucial to explain the performance between tasks. Thus, using this methodology we revealed a probable functional arrangement of neural systems engaged during different timing behaviors.     

Impairment of auditory-motor timing and compensatory reorganization after ventral premotor cortex stimulation

Integrating auditory and motor information often requires precise timing as in speech and music. In humans, the position of the ventral premotor cortex (PMv) in the dorsal auditory stream renders this area a node for auditory-motor integration. Yet, it remains unknown whether the PMv is critical for auditory-motor timing and which activity increases help to preserve task performance following its disruption. 16 healthy volunteers participated in two sessions with fMRI measured at baseline and following rTMS (rTMS) of either the left PMv or a control region. Subjects synchronized left or right finger tapping to sub-second beat rates of auditory rhythms in the experimental task, and produced self-paced tapping during spectrally matched auditory stimuli in the control task. Left PMv rTMS impaired auditory-motor synchronization accuracy in the first sub-block following stimulation (p<0.01, Bonferroni corrected), but spared motor timing and attention to task. Task-related activity increased in the homologue right PMv, but did not predict the behavioral effect of rTMS. In contrast, anterior midline cerebellum revealed most pronounced activity increase in less impaired subjects. The present findings suggest a critical role of the left PMv in feed-forward computations enabling accurate auditory-motor timing, which can be compensated by activity modulations in the cerebellum, but not in the homologue region contralateral to stimulation.     

Cross-modal distortion of time perception: demerging the effects of observed and performed motion

Temporal information is often contained in multi-sensory stimuli, but it is currently unknown how the brain combines e.g. visual and auditory cues into a coherent percept of time. The existing studies of cross-modal time perception mainly support the "modality appropriateness hypothesis", i.e. the domination of auditory temporal cues over visual ones because of the higher precision of audition for time perception. However, these studies suffer from methodical problems and conflicting results. We introduce a novel experimental paradigm to examine cross-modal time perception by combining an auditory time perception task with a visually guided motor task, requiring participants to follow an elliptic movement on a screen with a robotic manipulandum. We find that subjective duration is distorted according to the speed of visually observed movement: The faster the visual motion, the longer the perceived duration. In contrast, the actual execution of the arm movement does not contribute to this effect, but impairs discrimination performance by dual-task interference. We also show that additional training of the motor task attenuates the interference, but does not affect the distortion of subjective duration. The study demonstrates direct influence of visual motion on auditory temporal representations, which is independent of attentional modulation. At the same time, it provides causal support for the notion that time perception and continuous motor timing rely on separate mechanisms, a proposal that was formerly supported by correlational evidence only. The results constitute a counterexample to the modality appropriateness hypothesis and are best explained by Bayesian integration of modality-specific temporal information into a centralized "temporal hub".     

Expectation Suppression in Early Visual Cortex Depends on Task Set

Stimulus expectation can modulate neural responses in early sensory cortical regions, with expected stimuli often leading to a reduced neural response. However, it is unclear whether this expectation suppression is an automatic phenomenon or is instead dependent on the type of task a subject is engaged in. To investigate this, human subjects were presented with visual grating stimuli in the periphery that were either predictable or non-predictable while they performed three tasks that differently engaged cognitive resources. In two of the tasks, the predictable stimulus was task-irrelevant and spatial attention was engaged at fixation, with a high load on either perceptual or working memory resources. In the third task, the predictable stimulus was task-relevant, and therefore spatially attended. We observed that expectation suppression is dependent on the cognitive resources engaged by a subjects’ current task. When the grating was task-irrelevant, expectation suppression for predictable items was visible in retinotopically specific areas of early visual cortex (V1-V3) during the perceptual task, but it was abolished when working memory was loaded. When the grating was task-relevant and spatially attended, there was no significant effect of expectation in early visual cortex. These results suggest that expectation suppression is not an automatic phenomenon, but dependent on attentional state and type of available cognitive resources.     

Anodal tDCS over the Motor Cortex on Prepared and Unprepared Responses in Young Adults

Anodal transcranial direct current stimulation (tDCS) over the primary motor cortex (M1) has been proposed as a possible therapeutic rehabilitation technique for motor impairment. However, despite extensive investigation into the effects of anodal tDCS on motor output, there is little information on how anodal tDCS affects response processes. In this study, we used a cued go/nogo task with both directional and non-directional cues to assess the effects of anodal tDCS over the dominant (left) primary motor cortex on prepared and unprepared motor responses. Three experiments explored whether the effectiveness of tDCS varied with timing between stimulation and test. Healthy, right-handed young adults participated in a double-blind randomised controlled design with crossover of anodal tDCS and sham stimulation. In Experiment 1, twenty-four healthy young adults received anodal tDCS over dominant M1 at least 40 mins before task performance. In Experiment 2, eight participants received anodal tDCS directly before task performance. In Experiment 3, twenty participants received anodal tDCS during task performance. In all three experiments, participants responded faster to directional compared to non-directional cues and with their right hand. However, anodal tDCS had no effect on go/nogo task performance at any stimulation – test interval. Bayesian analysis confirmed that anodal stimulation had no effect on response speed. We conclude that anodal tDCS over M1 does not improve response speed of prepared or unprepared responses of young adults in a go/nogo task.     

A model of synchronization of motor acts to a stimulus sequence

A closed-loop timing model is proposed that accounts for several phenomena observed in tasks which require production of a sequence of motor acts in synchrony with a sequence of stimuli. In contrast to the previous models, variables available to the central nervous system of a subject (internal variables) and externally measurable variables are distinguished, and several physiologically justifiable internal variables are included. The model assumes the existence of (a) an internal time-keeper producing a reference interval that is used in a motor-control unit for timing of the next motor command; (b) an intrinsic (subjective) synchrony that relies on some a posteriori (feedback) information about the already executed onset of the motor act. A two-way error-corrective mechanism is hypothesized: (1) period (inverted frequency) corrections — the reference interval (period) is set at the beginning of the task according to the interstimulus-onset interval (s) and later corrected for differences between its duration and the actual duration of s; (2) phase corrections — internal synchronization errors (i.e., time gaps between the central temporal availability of internal representations of stimuli and of some feedback aspect of responses) are corrected for directly in the motor-control unit. Objectively measured systematic asynchrony of responses and stimuli is determined by the internal delays in information transduction. Finally, the model is used for making predictions of a subject's performance in some other experimental settings of the synchronization task.The core of this study was presented at the 4th Workshop on Rhythm Perception and Production, June 1992, Bourges, France (Mates 1992)     

Mirroring Pain in the Brain: Emotional Expression versus Motor Imitation

Perception of pain in others via facial expressions has been shown to involve brain areas responsive to self-pain, biological motion, as well as both performed and observed motor actions. Here, we investigated the involvement of these different regions during emotional and motor mirroring of pain expressions using a two-task paradigm, and including both observation and execution of the expressions. BOLD responses were measured as subjects watched video clips showing different intensities of pain expression and, after a variable delay, either expressed the amount of pain they perceived in the clips (pain task), or imitated the facial movements (movement task). In the pain task condition, pain coding involved overlapping activation across observation and execution in the anterior cingulate cortex, supplementary motor area, inferior frontal gyrus/anterior insula, and the inferior parietal lobule, and a pain-related increase (pain vs. neutral) in the anterior cingulate cortex/supplementary motor area, the right inferior frontal gyrus, and the postcentral gyrus. The ‘mirroring’ response was stronger in the inferior frontal gyrus and middle temporal gyrus/superior temporal sulcus during the pain task, and stronger in the inferior parietal lobule in the movement task. These results strongly suggest that while motor mirroring may contribute to the perception of pain expressions in others, interpreting these expressions in terms of pain content draws more heavily on networks involved in the perception of affective meaning.     

Prospective timing under dual-task paradigms: attentional and contextual-change mechanisms

The effect of a concurrent memory task on prospective time estimates by human participants was investigated in two experiments. The objective was to isolate task effects from those of participant timing strategy (self-paced counting) and number of contextual changes during the temporal stimulus. Accordingly, self-paced counting was suppressed by requiring participants to perform a word-reading task during the temporal stimuli, while number of stimulus changes presented during temporal stimuli was controlled. Presence versus absence of the concurrent memory task was manipulated in Experiment 1, and instruction to focus on timing or to focus on memory was manipulated in Experiment 2. There was no significant effect of presence versus absence of the concurrent memory task on time estimates; however, time estimates were shorter when participants were instructed to focus on memory versus timing. In both experiments, time estimates were positively correlated with participants' estimates of the number of words presented during the interval, even though number of words presented was invariant. These findings were generally consistent with resource-allocation attentional accounts of concurrent task effects; however, support for a contextual-change model of timing was also obtained.     

Temporal expectancy in the context of a theory of visual attention

Temporal expectation is expectation with respect to the timing of an event such as the appearance of a certain stimulus. In this paper, temporal expectancy is investigated in the context of the theory of visual attention (TVA), and we begin by summarizing the foundations of this theoretical framework. Next, we present a parametric experiment exploring the effects of temporal expectation on perceptual processing speed in cued single-stimulus letter recognition with unspeeded motor responses. The length of the cue–stimulus foreperiod was exponentially distributed with one of six hazard rates varying between blocks. We hypothesized that this manipulation would result in a distinct temporal expectation in each hazard rate condition. Stimulus exposures were varied such that both the temporal threshold of conscious perception (t₀ ms) and the perceptual processing speed (v letters s⁻¹) could be estimated using TVA. We found that the temporal threshold t₀ was unaffected by temporal expectation, but the perceptual processing speed v was a strikingly linear function of the logarithm of the hazard rate of the stimulus presentation. We argue that the effects on the v values were generated by changes in perceptual biases, suggesting that our perceptual biases are directly related to our temporal expectations.     

The neural representation of time

This review summarizes recent investigations of temporal processing. We focus on motor and perceptual tasks in which crucial events span hundreds of milliseconds. One key question concerns whether the representation of temporal information is dependent on a specialized system, distributed across a network of neural regions, or computed in a local task-dependent manner. Consistent with the specialized system framework, the cerebellum is associated with various tasks that require precise timing. Computational models of timing mechanisms within the cerebellar cortex are beginning to motivate physiological studies. Emphasis has also been placed on the basal ganglia as a specialized timing system, particularly for longer intervals. We outline an alternative hypothesis in which this structure is associated with decision processes.     

Catching a ball at the right time and place: individual factors matter

Intercepting a moving object requires accurate spatio-temporal control. Several studies have investigated how the CNS copes with such a challenging task, focusing on the nature of the information used to extract target motion parameters and on the identification of general control strategies. In the present study we provide evidence that the right time and place of the collision is not univocally specified by the CNS for a given target motion; instead, different but equally successful solutions can be adopted by different subjects when task constraints are loose. We characterized arm kinematics of fourteen subjects and performed a detailed analysis on a subset of six subjects who showed comparable success rates when asked to catch a flying ball in three dimensional space. Balls were projected by an actuated launching apparatus in order to obtain different arrival flight time and height conditions. Inter-individual variability was observed in several kinematic parameters, such as wrist trajectory, wrist velocity profile, timing and spatial distribution of the impact point, upper limb posture, trunk motion, and submovement decomposition. Individual idiosyncratic behaviors were consistent across different ball flight time conditions and across two experimental sessions carried out at one year distance. These results highlight the importance of a systematic characterization of individual factors in the study of interceptive tasks.     

Trading Speed and Accuracy by Coding Time: A Coupled-circuit Cortical Model

Our actions take place in space and time, but despite the role of time in decision theory and the growing acknowledgement that the encoding of time is crucial to behaviour, few studies have considered the interactions between neural codes for objects in space and for elapsed time during perceptual decisions. The speed-accuracy trade-off (SAT) provides a window into spatiotemporal interactions. Our hypothesis is that temporal coding determines the rate at which spatial evidence is integrated, controlling the SAT by gain modulation. Here, we propose that local cortical circuits are inherently suited to the relevant spatial and temporal coding. In simulations of an interval estimation task, we use a generic local-circuit model to encode time by ‘climbing’ activity, seen in cortex during tasks with a timing requirement. The model is a network of simulated pyramidal cells and inhibitory interneurons, connected by conductance synapses. A simple learning rule enables the network to quickly produce new interval estimates, which show signature characteristics of estimates by experimental subjects. Analysis of network dynamics formally characterizes this generic, local-circuit timing mechanism. In simulations of a perceptual decision task, we couple two such networks. Network function is determined only by spatial selectivity and NMDA receptor conductance strength; all other parameters are identical. To trade speed and accuracy, the timing network simply learns longer or shorter intervals, driving the rate of downstream decision processing by spatially non-selective input, an established form of gain modulation. Like the timing network''s interval estimates, decision times show signature characteristics of those by experimental subjects. Overall, we propose, demonstrate and analyse a generic mechanism for timing, a generic mechanism for modulation of decision processing by temporal codes, and we make predictions for experimental verification.     

Independent coding of movement duration in a repetitive non-visually guided movement

Temporal information is an embedded feature of our sensory and motor experiences. How is temporal information encoded in the brain? In the two-stage theory of timing, an explicit representation of timing is responsible for the movement initiation while movement duration is coded implicitly. We investigated the correlation of movement duration and amplitude in a repetitive one-dimensional non-visually guided movement to find out if temporal information could be coded independently from movement. Subjects were asked to learn the distance between two points by moving their hands repeatedly along the distance between two sticks, while they could not see their hands and hand path. After a training phase, a delay of either 2 or 20 s was imposed and the subjects were asked to reproduce the learned distance. There was no correlation between distance difference and time difference in either delay condition. In the 20 s delay experiment, in comparison to the 2 s delay experiment, there was a significant increase in distance reproduction error. However, there was no significant change in time differences in either of the experiments. In addition, the time difference between the training and test trials was independent from the direction of the distance difference (i.e., overshot, undershot, or accurate). In conclusion, time may be coded as an independent measure after the delay period, so it should be a kind of explicitly coded information.