Rebecca M. C. Spencer

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.

Processing of Emotional Reactivity and Emotional Memory over Sleep

Sleep enhances memories, particularly emotional memories. As such, it has been suggested that sleep deprivation may reduce posttraumatic stress disorder. This presumes that emotional memory consolidation is paralleled by a reduction in emotional reactivity, an association that has not yet been examined. In the present experiment, we used an incidental memory task in humans and obtained valence and arousal ratings during two sessions separated either by 12 h of daytime wake or 12 h including overnight sleep. Recognition accuracy was greater following sleep relative to wake for both negative and neutral pictures. While emotional reactivity to negative pictures was greatly reduced over wake, the negative emotional response was relatively preserved over sleep. Moreover, protection of emotional reactivity was associated with greater time in REM sleep. Recognition accuracy, however, was not associated with REM. Thus, we provide the first evidence that sleep enhances emotional memory while preserving emotional reactivity.

Age-related changes in the cognitive function of sleep.

Healthy aging is characterized by a diminished quality of sleep with decreased sleep duration and increased time awake after sleep onset. Older adults awaken more frequently and tend to awaken less from rapid eye movement (REM) sleep and more from non-REM (nREM) sleep than young adults. Sleep architecture also begins changing in middle age leading to a dramatic decrease in the deepest stage of nREM-slow wave sleep (SWS)-as aging progresses. Other less marked nREM changes include reduced numbers of sleep spindles and K-complexes. In contrast, the amount of REM diminishes only slightly. Both circadian and homeostatic sleep-regulatory processes are affected by aging. Circadian rhythms of temperature, melatonin, and cortisol are phase advanced and their amplitude diminished. An increased number of nocturnal awakenings and diminished daytime sleepiness suggest diminished homeostatic sleep pressure. A variety of endocrine and neuromodulatory changes (e.g., reduced growth hormone and dopamine levels) also accompany healthy aging. Healthy aging is characterized by declines in working memory and new episodic memory performance with relative sparing of semantic memory, recognition memory, and priming. Memory systems impacted by aging are associated with volumetric and functional changes in fronto-striatal circuits along with more limited changes in medial temporal structures (in which larger aging-related changes suggest neuropathology). Cross-sectional studies generally associate poorer sleep quality with poorer neuropsychological functioning. However, paradoxically, older adults appear to be more resistant to the cognitive effects of sleep deprivation, restriction, and fragmentation than younger adults. A new and expanding field examines the interaction between aging and sleep-dependent memory consolidation. Among forms of learning displaying prominent sleep-dependent consolidation in young adults, motor-sequence learning displays loss of sleep-dependent consolidation with aging whereas sleep-dependent consolidation of verbal declarative memory appears spared. Findings suggest that improving sleep through behavioral or pharmacological treatments may enhance cognition and performance in older adults.

Comparison of patients with Parkinson's disease or cerebellar lesions in the production of periodic movements involving event-based or emergent timing

We have hypothesized a distinction between the processes required to control the timing of different classes of periodic movements. In one class, salient events mark successive cycles. For these movements, we hypothesize that the temporal goal is a requisite component of the task representation, what we refer to as event-based timing. In the other class, the successive cycles are produced continuously. For these movements, alternative control strategies can optimize performance, allowing timing to be emergent. In a previous study, patients with cerebellar lesions were found to be selectively impaired on event-based timing tasks; they were unimpaired on a continuously produced task. In the present study, patients with Parkinsons disease were tested on repetitive movement tasks in which timing was either event-based or emergent. Temporal variability on either type of task did not differ between on- and off-medication sessions for the Parkinsons patients nor did patient performance differ from that of controls. These results suggest that the basal ganglia play a minimal role in movement timing and that impairments on event-based timing tasks are specific to cerebellar damage.

Sleep-Dependent Consolidation of Contextual Learning

Memory consolidation is facilitated by sleep. Specifying the functional domain of sleep-dependent consolidation (SDC) is important for identifying the neural mechanisms underlying this phenomenon. Previous work indicates that SDC may be limited to conditions in which learning is explicit. In the present study, we tested the hypothesis that SDC may also occur with implicit learning when learning benefits from the formation of contextual associations, a function associated with the hippocampus. Three versions of the serial-reaction-time task (SRTT) were examined, and SDC was assessed by comparing performance after 12 hr breaks that included or did not include sleep. SDC was observed in the Explicit condition. Two implicit conditions were compared. In the Implicit Noncontextual condition, participants performed a concurrent tone-counting task with the pitch of each tone selected at random, precluding cross-dimensional associations. In the Implicit Contextual condition, participants responded to the color of the cues while the spatial location of the cues followed a correlated sequence. Whereas learning was observed in both implicit conditions, SDC was restricted to the contextual condition. Given that the formation of contextual associations is dependent on the hippocampus, we suggest that SDC is a hippocampus-mediated process.

Sleep modulates word-pair learning but not motor sequence learning in healthy older adults

Sleep benefits memory across a range of tasks for young adults. However, remarkably little is known of the role of sleep on memory for healthy older adults. We used 2 tasks, 1 assaying motor skill learning and the other assaying nonmotor/declarative learning, to examine off-line changes in performance in young (20-34 years), middle-aged (35-50 years), and older (51-70 years) adults without disordered sleep. During an initial session, conducted either in the morning or evening, participants learned a motor sequence and a list of word pairs. Memory tests were given twice, 12 and 24 hours after training, allowing us to analyze off-line consolidation after a break that included sleep or normal wake. Sleep-dependent performance changes were reduced in older adults on the motor sequence learning task. In contrast, sleep-dependent performance changes were similar for all 3 age groups on the word pair learning task. Age-related changes in sleep or networks activated during encoding or during sleep may contribute to age-related declines in motor sequence consolidation. Interestingly, these changes do not affect declarative memory.

Sleep spindles in midday naps enhance learning in preschool children

Significance Lacking scientific understanding of the function of naps in early childhood, policy makers may curtail preschool classroom nap opportunities due to increasing curriculum demands. Here we show evidence that classroom naps support learning in preschool children by enhancing memories acquired earlier in the day as compared with equivalent intervals spent awake. Despite the fact that midday naps are characteristic of early childhood, very little is understood about the structure and function of these sleep bouts. Given that sleep benefits memory in young adults, it is possible that naps serve a similar function for young children. However, children transition from biphasic to monophasic sleep patterns in early childhood, eliminating the nap from their daily sleep schedule. As such, naps may contain mostly light sleep stages and serve little function for learning and memory during this transitional age. Lacking scientific understanding of the function of naps in early childhood, policy makers may eliminate preschool classroom nap opportunities due to increasing curriculum demands. Here we show evidence that classroom naps support learning in preschool children by enhancing memories acquired earlier in the day compared with equivalent intervals spent awake. This nap benefit is greatest for children who nap habitually, regardless of age. Performance losses when nap-deprived are not recovered during subsequent overnight sleep. Physiological recordings of naps support a role of sleep spindles in memory performance. These results suggest that distributed sleep is critical in early learning; when short-term memory stores are limited, memory consolidation must take place frequently.

Cerebellar activation during discrete and not continuous timed movements: an fMRI study.

Individuals with cerebellar lesions are impaired in the timing of repetitive movements that involve the concatenation of discrete events such as tapping a finger. In contrast, these individuals perform comparably to controls when producing continuous repetitive movements. Based on this, we have proposed that the cerebellum plays a key role in event timing-the representation of the temporal relationship between salient events related to the movement (e.g., flexion onset or contact with a response surface). In the current study, we used fMRI to examine cerebellar activity during discrete and continuous rhythmic movements. Participants produced rhythmic movements with the index finger either making smooth, continuous transitions between flexion and extension or with a pause inserted before each flexion phase making the movement discrete. Lateral regions in lobule VI, ipsilateral to the moving hand were activated in a similar manner for both conditions. However, activation in the superior vermis was significantly greater when the movements were discrete compared to when the movements were continuous. This pattern was not evident in cortical regions within the field of view, including M1 and SMA. The results are consistent with the hypothesis that subregions of the cerebellum are selectively engaged during tasks involving event timing.

Evidence of a Novel Somatopic Map in the Human Neocerebellum During Complex Actions

The human neocerebellum has been hypothesized to contribute to many high-level cognitive processes including attention, language, and working memory. Support for these nonmotor hypotheses comes from evidence demonstrating structural and functional connectivity between the lateral cerebellum and cortical association areas as well as a lack of somatotopy in lobules VI and VII, a hallmark of motor representations in other areas of the cerebellum and cerebral cortex. We set out to test whether somatotopy exists in these lobules by using functional magnetic resonance imaging to measure cerebellar activity while participants produced simple or complex movements, using either fingers or toes. We observed a previously undiscovered somatotopic organization in neocerebellar lobules VI and VIIA that was most prominent when participants executed complex movements. In contrast, activation in the anterior lobe showed a similar somatotopic organization for both simple and complex movements. While the anterior somatotopic representation responded selectively during ipsilateral movements, the new cerebellar map responded during both ipsi- and contralateral movements. The presence of a bilateral, task-dependent somatotopic map in the neocerebellum emphasizes an important role for this region in the control of skilled actions.

Timing Variability in Circle Drawing and Tapping: Probing the Relationship Between Event and Emergent Timing

R. Ivry, R. M. Spencer, H. N. Zelaznik, and J. Diedrichsen (2002) have proposed a distinction between timed movements in which a temporal representation is part of the task goal (event timing) and those in which timing properties are emergent. The issue addressed in the present experiment was how timing in conditions conducive to emergent timing becomes established. According to what the authors term the transformation hypothesis, timing initially requires an event-based representation when the temporal goal is defined externally (e.g., by a metronome), but over the first few movement cycles, control processes become established that allow timing to become emergent. Different groups of participants (N = 84) executed either 1 timed interval, 4 timed intervals, or 2 timed intervals separated by a pause. They produced the intervals by either circle drawing, a task associated with emergent timing, or tapping, a task associated with event timing. Analyses of movement variability suggested that similar timing processes were used in the 2 tasks only during the 1st interval. Those results are consistent with the transformation hypothesis and lead to the inference that the transition from event-based control to emergent timing can occur rapidly during continuous movements.