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Abstract
The major tenets of beat-frequency/coincidence-detection models of reward-related timing are reviewed in light of recent behavioral and neurobiological findings. This includes the emphasis on a core timing network embedded in the motor system that is comprised of a corticothalamic-basal ganglia circuit. Therein, a central hub provides timing pulses (i.e., predictive signals) to the entire brain, including a set of distributed satellite regions in the cerebellum, cortex, amygdala, and hippocampus that are selectively engaged in timing in a manner that is more dependent upon the specific sensory, behavioral, and contextual requirements of the task. Oscillation/coincidence-detection models also emphasize the importance of a tuned ‘perception’ learning and memory system whereby target durations are detected by striatal networks of medium spiny neurons (MSNs) through the coincidental activation of different neural populations, typically utilizing patterns of oscillatory input from the cortex and thalamus or derivations thereof (e.g., population coding) as a time base. The measure of success of beat-frequency/coincidence-detection accounts, such as the Striatal Beat-Frequency model of reward-related timing (SBF), is their ability to accommodate new experimental findings while maintaining their original framework, thereby making testable experimental predictions concerning diagnosis and treatment of issues related to a variety of dopamine-dependent basal ganglia disorders, including Huntington’s and Parkinson’s disease.
Discriminative fear conditioning requires learning to dissociate between safety cues and cues that predict negative outcomes yet little is known about what processes contribute to discriminative fear learning. According to attentional models of time perception, processes that distract from timing result in temporal underestimation. If discriminative fear learning only requires learning what cues predict what outcomes, and threatening stimuli distract attention from timing, then better discriminative fear learning should predict greater temporal distortion on threat trials. Alternatively, if discriminative fear learning also reflects a more accurate perceptual experience of time in threatening contexts, discriminative fear learning scores would predict less temporal distortion on threat trials, as time is perceived more veridically. Healthy young adults completed discriminative fear conditioning in which they learned to associate one stimulus (CS+) with aversive electrical stimulation and another stimulus (CS−) with non-aversive tactile stimulation and then an ordinal-comparison timing task during which CSs were presented as task-irrelevant distractors. Consistent with predictions, we found an overall temporal underestimation bias on CS+ relative to CS− trials. Differential skin conductance responses to the CS+ versus the CS− during conditioning served as a physiological index of discriminative fear conditioning and this measure predicted the magnitude of the underestimation bias, such that individuals exhibiting greater discriminative fear conditioning showed less underestimation on CS+ versus CS− trials. These results are discussed with respect to the nature of discriminative fear learning and the relationship between temporal distortions and maladaptive threat processing in anxiety.
Abstract
One of the major challenges for computational models of timing and time perception is to identify a neurobiological plausible implementation that predicts various behavioral properties, including the scalar property and retrospective timing. The available timing models primarily focus on the scalar property and prospective timing, while virtually ignoring the computational accessibility. Here, we first selectively review timing models based on ramping activity, oscillatory pattern, and time cells, and discuss potential challenges for the existing models. We then propose a multifrequency oscillatory model that offers computational accessibility, which could account for a much broader range of timing features, including both retrospective and prospective timing.
Basic mechanisms of interval timing and associative learning are shared by many animal species, and develop quickly in early life, particularly across infancy, and childhood. Indeed, John Wearden in his book “The Psychology of Time Perception”, which is based on decades of his own research with colleagues, and which our commentary serves to primarily review, has been instrumental in implementing animal models and methods in children and adults, and has revealed important similarities (and differences) between human timing (and that of animals) when considered within the context of scalar timing theory. These seminal studies provide a firm foundation upon which the contemporary multifaceted field of timing and time perception has since advanced. The contents of the book are arguably one piece of a larger puzzle, and as Wearden cautions, “The reader is warned that my own contribution to the field has been exaggerated here, but if you are not interested in your own work, why would anyone else be?” Surely there will be many interested readers, however the book is noticeably lacking in it neurobiological perspective. The mind (however it is conceived) needs a brain (even if behaviorists tend to say “the brain behaves”, and most neuroscientists currently have a tenuous grasp on the neural mechanisms of temporal cognition), and to truly understand the psychology of time, brain and behavior must go hand in hand regardless of the twists, turns, and detours along the way.
Male Sprague–Dawley rats were exposed to social defeat and subordination by aggressive male Long–Evans rats. The social defeat procedure involved the continuous exposure to an aggressive resident for 10 days, while living in a protective cage within the resident’s home cage with daily brief confrontations. These stress experiences resulted in 1) reduced body weight; 2) decreased social interaction; 3) increased ultrasonic vocalizations; 4) reduced sucrose preference (anhedonia); and 5) decreased clock speed while timing 15-s and 45-s target durations in a bi-peak procedure. Treatment with ketamine (15 mg/kg, i.p.) produced a rapid reversal of anhedonia and overproduction of duration. Taken together, these data provide the first evaluation of the effects of continuous social defeat and its associated depression-like symptoms on timing and time perception using a ‘state change’ design.
Bilateral intratympanic sodium arsenate injections (100 mg/ml in isotonic saline) in adult male Long Evans rats produced impairments in allocentric navigation using a 12-arm radial maze procedure as well as a motor test battery designed to evaluate vestibular function. In contrast, no impairments in the accuracy or precision of duration reproduction using 20-s and 80-s peak-interval procedures were observed when both target durations were associated with the same lever response, but distinguished by signal modality (e.g., light or sound). In contrast, an ordinal-reproduction procedure with 800, 3200, and 12,800 ms standards requiring the timing of self-initiated movements during the production phase revealed large impairments in the accuracy and precision of timing for vestibular lesioned rats. These impairments were greater on trials in which self-initiated body movements (e.g., holding down the response lever for a fixed duration) were required without the support of external stimuli signaling the onset and offset of the reproduced duration in contrast to trials in which such external support was provided. The conclusion is that space and time are separable entities and not simply the product of a generalized system, but they can be integrated into a common metric using gravity and self-initiated movement as a reference.