Neural Repetition Suppression Modulates Time Perception: Evidence From Electrophysiology and Pupillometry

Human time perception is malleable and subject to many biases. For example, it has repeatedly been shown that stimuli that are physically intense or that are unexpected seem to last longer. Two competing hypotheses have been proposed to account for such biases: One states that these temporal illusions are the result of increased levels of arousal that speeds up neural clock dynamics, whereas the alternative “magnitude coding” account states that the magnitude of sensory responses causally modulates perceived durations. Common experimental paradigms used to study temporal biases cannot dissociate between these accounts, as arousal and sensory magnitude covary and modulate each other. Here, we present two temporal discrimination experiments where two flashing stimuli demarcated the start and end of a to-be-timed interval. These stimuli could be either in the same or a different location, which led to different sensory responses because of neural repetition suppression. Crucially, changes and repetitions were fully predictable, which allowed us to explore effects of sensory response magnitude without changes in arousal or surprise. Intervals with changing markers were perceived as lasting longer than those with repeating markers. We measured EEG (Experiment 1) and pupil size (Experiment 2) and found that temporal perception was related to changes in ERPs (P2) and pupil constriction, both of which have been related to responses in the sensory cortex. Conversely, correlates of surprise and arousal (P3 amplitude and pupil dilation) were unaffected by stimulus repetitions and changes. These results demonstrate, for the first time, that sensory magnitude affects time perception even under constant levels of arousal.

Neural repetition suppression modulates time perception: evidence from electrophysiology and pupillometry

Human time perception is malleable and subject to many biases. For example, it has repeatedly been shown that stimuli that are physically intense or that are unexpected seem to last longer. Two competing hypotheses have been proposed to account for such biases: one states that these temporal illusions are the result of increased levels of arousal which speeds up neural clock dynamics, whereas the alternative ‘magnitude coding’ account states that the magnitude of sensory responses causally modulates perceived durations. Common experimental paradigms used to study temporal biases can not dissociate between these accounts, as arousal and sensory magnitude covary and modulate each other. Here, we present two temporal discrimination experiments where two flashing stimuli demarcated the start and end of a to-be-timed interval. These stimuli could either be in the same or in a different location, which led to different sensory responses due to neural repetition suppression. Crucially, changes and repetitions were fully predictable, which allowed us explore effects of sensory response magnitude without impacting arousal or surprise. Intervals with changing markers were perceived as lasting longer than those with repeating markers. We measured EEG (Experiment 1) and pupil size (Experiment 2), and found that temporal perception was related to changes in event-related potentials (P2) and pupil constriction, both of which have been related to responses in sensory cortex. Conversely, correlates of surprise and arousal (P3 amplitude and pupil dilation) were unaffected by stimulus repetitions and changes. These results demonstrate, for the first time, that sensory magnitude affects time perception even under constant levels of arousal.

Tactile detection of a dot on a smooth surface: peripheral neural events

The capacities of humans to detect the presence of a single raised dot of 550 micron diameter on a smooth plate and to judge the magnitude of evoked sensation were determined for dots of different heights, stroked at different velocities across the passive fingerpad. Evoked responses to the same stimuli were recorded from single, slowly adapting (SA), rapidly adapting (RA), and Pacinian (PC) mechanoreceptive peripheral nerve fibers innervating the fingerpad of anesthetized macaque monkeys. When the stroke velocity was 10 mm/s, dot height detection thresholds, as determined from measurements of detection sensitivity were between 1 and 3 microns for all human observers. From fiber recordings in monkeys, the RAs had dot height thresholds of 2-4 microns, i.e., within the range of human detection thresholds. The dot height thresholds were 8 microns or greater for SAs and 21 micron or greater for PCs. In contrast, force thresholds for punctate von Frey filaments did not differ for RAs and SAs and were lowest for PCs. The magnitude of sensation evoked in human increased with increases in dot height above threshold. Similarly, the number of nerve impulses evoked in monkey RAs increased with dot height as did the widths of RA receptive fields. Neither changes in stroke velocity from 10 to 40 mm/s nor changes in vertical force applied by the dot plate to the skin altered sensory magnitude evoked by a 15-microns high dot or the number of impulses evoked in RAs. However, a decrease in stroke velocity from 10 to 1.5 mm/s elevated sensory detection thresholds and, for the 15-microns high dot, decreased sensory magnitude, the number of impulses in RAs, and the widths of RA receptive fields. It was hypothesized that the mechanical event responsible for activating the RA was the lateral deformation of elevated regions of skin. In support of this, the number of impulses evoked in RAs by a dot was greater when the dot was stroked across, as opposed to along, the papillary ridges. Also, under certain stimulus conditions, a correspondence was observed between the occurrence of each action potential in an RA and the passage of the leading edge of the dot across the peak of a papillary ridge. It is concluded that the responses of RAs alone account for the sensory capacity to detect a dot of minimal height on a smooth surface with the fingerpad.(ABSTRACT TRUNCATED AT 400 WORDS)

Effect of frequency on perceived magnitude of added loads to breathing

Using open-magnitude scaling, six normal subjects estimated the perceived magnitude of a range of added elastic loads (20–76 cmH2O/l), applied for a sequence of five breaths, at frequencies varying from 5 to 26.4 breaths/min. Two experiments were performed. In the first, frequency was increased by a reduction in expiratory duration (TE), and the duty cycle (ratio of inspiratory duration to total breath duration, TI/TT) ranged between 0.10 and 0.52. The perceived magnitude psi increased significantly with the peak airway pressure (Pm) (P less than 0.0001) but did not reach conventional significance with frequency (fb) (P = 0.15): psi = K0Pm1.23fb0.07 (r = 0.911). However, the sensory magnitude increased significantly as the duty cycle increased (P less than 0.01), but when it was included, the magnitude decreased minimally with frequency (P less than 0.01): psi = K0Pm1.3fb-0.97 TI/TT1.14 (r = 0.92). In the second experiment the duty cycle (TI/TT) was kept constant [(0.43 +/- 0.008 (SE)] and frequency (5–26.4 breaths/min) increased at the expense of shortening both TI and TE. The perceived magnitude of the added elastances decreased with the increase in frequency. However, when the perceived magnitude was corrected for the duration of inspiration, which is known to increase the sensory magnitude, psi = K0Pm1.3TI0.56, the sensory magnitude increased significantly with frequency (P less than 0.001): psi/TI0.56 = K0Pm1.21fb0.28 (r = 0.773). The decrease in inspiratory duration had a greater quantitative effect decreasing sensory magnitude than frequency had on increasing the magnitude. The effect of increasing frequency is complex and depends on the simultaneous intensity, duration of inspiratory pressure, and the duty cycle.

Psychophysics of inspiratory muscle force

The perceived magnitude of static inspiratory muscle pressure was studied in normal subjects using psychophysical techniques. The sensory magnitude of a range of inspiratory pressures increased as the magnitude of the pressure increased. When the duration of the inspiratory pressure was controlled, the sensory magnitude also increased as duration increased. The relationship can be described by a single psychophysical function, psi = k x P1.234 x t0.62, where psi is perceived magnitude, P is inspiratory pressure, t is duration, and k is a constant. Use of different muscle groups and changes in lung volume altered the perceived magnitude of static inspiratory pressures. When static inspiratory pressures were generated by the abdomen-diaphragm, the perceived magnitude was significantly greater (P less than 0.01) than when they were generated by the rib cage. When lung volume was increased, the perceived magnitude of pressure was reduced. The results show that the perceived magnitude of static inspiratory pressures is affected by the pressure itself, pressure duration, the muscles used, and the lung volume at which the pressure is generated.

Effect of ventilatory drive on the perceived magnitude of added loads to breathing

Using open-magnitude scaling we studied the importance of ventilatory drive on the perceived magnitude of respiratory loads by applying a range of externally added resistances (2.1–77.1 cmH2O X l-1 X s) to normal subjects at rest and at three increasing levels of ventilatory drive induced by exercise, CO2-stimulated breathing, and hypoxia. Under all conditions studied the perceived magnitude of the added loads increased with the magnitude of the resistive load and as the underlying level of ventilatory drive increased. When the results were expressed in terms of peak inspiratory pressure, the perceived magnitude was related to the magnitude of the peak inspiratory pressure by a power function (mean r = 0.97). These results suggest that the perceived magnitude of added resistive loads increased with increasing ventilatory drive, in such a manner that the increase in sensory magnitude is proportional to the increase in the inspiratory muscle force developed and suggests that something dependent on this force mediates the sensation.