Effects of stimulus and task structure on temporal perceptual learning.

Our ability to discriminate temporal intervals can be improved with practice. This learning is generally thought to reflect an enhancement in the representation of a trained interval, which leads to interval-specific improvements in temporal discrimination. In the present study, we asked whether temporal learning is further constrained by context-specific factors dictated through the trained stimulus and task structure. Two groups of participants were trained using a single-interval auditory discrimination task over 5 days. Training intervals were either one of eight predetermined values (FI group), or random from trial to trial (RI group). Before and after the training period, we measured discrimination performance using an untrained two-interval temporal comparison task. Our results revealed a selective improvement in the FI group, but not the RI group. However, this learning did not generalize between the trained and untrained tasks. These results highlight the sensitivity of TPL to stimulus and task structure, suggesting that mechanisms of temporal learning rely on processes beyond changes in interval representation.

The quantification of behavior in the presence of compound stimuli.

Animals live in complex environments where multiple cues can provide consistent or conflicting information about how to behave most effectively. Previous research has described how animals combine information with qualitative combination rules; the goal of this article was to quantify the combination rule used by rats when 2 previously trained stimuli of separate modalities were presented simultaneously. Rats in a lever box were trained with 2 stimuli (light and tone) assigned given probabilities of food before they were tested in compound. Changes in the probability of food assigned to each stimulus produced linear changes in the rat's rate of responding to these stimuli, both when the stimuli were presented individually and in compound. Using a linear regression, 3 features of the stimuli (rate of reinforcement, probability of food, and rate of responding) were compared to see which accounted for behavior in the presence of the compound best; z-scores were used to account for between rat variability. The linear regression allows for direct comparisons to be made regarding what may be combined under these conditions; something many behavioral models cannot. Our analysis suggests that rats weigh each stimulus of the compound differentially. More specifically, they weigh the stimulus that had more frequent changes to the assigned probability of food more than the stimulus whose probability of food remained more consistent across phases of the experiment. (PsycINFO Database Record

Optimal response rates in humans and rats.

The analysis of response rates has been highly influential in psychology, giving rise to many prominent theories of learning. There is, however, growing interest in explaining response rates, not as a global response to associations or value, but as a decision about how to space responses in time. Recently, researchers have shown that humans and mice can time a single response optimally; that is, in a way that maximizes reward. Here, we use the well-established differential reinforcement of low rates (DRL) timing task to show that humans and rats come close to optimizing reinforcement rate, but respond systematically faster than they should.

Integrating timing and conditioning approaches to study behavior.

Skinner and Pavlov had innovative ways to measure both the times of their subject's responses, as well as the rate of their responses. Since then, different subfields within the study of animal behavior have prioritized either the rate or timing of responses, creating a divide in data and theory. Both timing and conditioning fields have proven fruitful, producing large bodies of empirical data and developing sophisticated models. Despite their individual successes, a unified view of simple behavior is still lacking. This may be caused, at least in part, by the differential emphasis on data collection and analysis techniques. The result is that these subfields produce models that fit their data well, but fail to translate to the other domain. This is startling given the fact that both subfields use nearly identical experimental procedures. To highlight similarities within the subfields, and provide empirical data in support of this integration, 18 Sprague-Dawley rats were trained on trace, delay, and backward conditioning procedures. Using these empirical data we discuss how traditional summary measures used by these subfields can be limiting, and suggest methods that may aid in the integration of these subfields toward common goals.

Amyloid-beta accumulation, neurogenesis, behavior, and the age of rats.

The goals of this research were to describe age-related changes in brain biochemistry and behavior, and the relationships between them. The chronological ages of greatest change are particularly important for targeting interventions. In this experiment, 36 Fischer 344/Brown-Norway rats (3, 12, 20, and 30 months old) were trained in lever boxes on temporal discrimination tasks. The greatest response rate decrease and response pattern change occurred between 12 and 20 months. The biochemical results showed that amyloid-beta peptides (Aß40 and Aß42) increased with age. The endothelial expression of the Aß influx transporter (RAGE) also increased, and the expression of Aß efflux transporter (LPR-1) decreased, with age. The greatest change in the biochemical measures also were between 12 and 20 months. Twenty additional rats were analyzed for stem cell proliferation, and neurogenesis decreased with age, particularly between about 12 and 20 months. These early changes in brain, biochemistry, and behavior provide opportunity for new therapies or prophylaxis.

Brief stimuli as context.

Context may be defined as a stimulus that provides global information about the reinforcement rate in the current environment. Twenty-four rats were trained in lever boxes with different stimuli serving as context on different sessions. The goal of the first experiment was to determine whether or not brief stimuli provide global information as effectively as continuous stimuli. The sessions contained brief stimuli at random times throughout the sessions, a continuous stimulus throughout the session, both brief and continuous stimuli, or neither. Results indicated that brief and continuous stimuli provided similar global information (i.e., they served as contextual stimuli). The goal of the second experiment was to determine the differential effects brief stimuli have on behavior when they provide either global or local information. The conclusion was that stimuli that provide local information regarding the time of reinforcement affect the time of responses, and that stimuli that provide global information affect response rate. This article is part of a Special Issue entitled: insert SI title.

A resolution of the debate about associative and temporal learning.

For more than a century, there has been an extensive experimental literature on both associative and temporal learning. Associative learning is based on strength of associations between elements. In contrast, temporal learning is based on durations of intervals between time markers. The same procedures have often been used to examine the formation of associative bonds between elements and to examine the learning of durations between time markers. Although there is general agreement on the behavioral results, different computational models of associative and temporal learning have led to a lengthy debate regarding whether associations between elements or interval durations account for these results. The purpose of this article is to propose a resolution that requires the development and evaluation of a computational model of procedures that produce associative and/or temporal learning. Standard methods of goodness-of-fit, simplicity, and generality can be supplemented by Turing tests to determine the extent to which a computer algorithm can predict whether the behavior came from the animal or the model. A successful general model should help guide the development of specific alternative models.

Bayesian optimization of time perception.

Precise timing is crucial to decision-making and behavioral control, yet subjective time can be easily distorted by various temporal contexts. Application of a Bayesian framework to various forms of contextual calibration reveals that, contrary to popular belief, contextual biases in timing help to optimize overall performance under noisy conditions. Here, we review recent progress in understanding these forms of temporal calibration, and integrate a Bayesian framework with information-processing models of timing. We show that the essential components of a Bayesian framework are closely related to the clock, memory, and decision stages used by these models, and that such an integrated framework offers a new perspective on distortions in timing and time perception that are otherwise difficult to explain.

Hippocampus, time, and memory.

Five experiments were conducted to determine the effects of hippocampal damage on timing and the memory for temporal events. In Experiments 1-3, rats were trained to discriminate between auditory signals that differed in both duration (2 or 8 s) and rate (2 or 16 cycles/s). Half of the rats were trained to discriminate duration, and half were trained to discriminate rate. After rats acquired the relevant discrimination, signals with intermediate durations and rates were presented to obtain psychophysical functions that related signal duration and/or rate to response choice. Rats then received either lesions of the fimbria-fornix or control operations. Postoperatively, the accuracy of duration and rate discriminations as measured by the difference limen (DL) was unaffected by the lesion, but the point of subjective equality (PSE) was shifted to a shorter duration and a slower rate by the lesion in Experiment 1. Both rats with lesions and rats with control operations showed cross-modal transfer of duration and rate from the auditory signals used in training to visual signals used in testing in Experiment 2. A 5-s delay was imposed between the end of a signal and the opportunity to respond in Experiment 3. The delay served as a retention interval for the rats trained in the rate discrimination, and the rats with fimbria-fornix lesions were selectively impaired by the addition of the delay as measured by an increase in the DL. The delay did not serve as a retention interval for rats trained in the duration discrimination because they were able to continue timing through the delay. A peak procedure was employed in Experiment 4. The maximum response rate of control rats was approximately at the time of scheduled reinforcement (20 s), but the maximum response rate of rats with fimbria-fornix lesions was reliably earlier than the time of scheduled reinforcement. When a 5-s gap was imposed in the signal, control rats summed the signal durations before and after the gap, whereas rats with fimbria-fornix lesions showed no retention of the signal duration prior to the gap. Experiment 5 continued the testing of the rats used in Experiments 1-4 and showed that rats with lesions had an impairment in a test of spatial working memory in an eight-arm radial maze. Taken together, these results demonstrate that a fimbria-fornix lesion interferes with temporal and spatial working memory, reduces the remembered time of reinforcement stored in reference memory, and has no effect on the animal's sensitivity to stimulus duration.

Hippocampus, time, and memory--a retrospective analysis.

In 1984, there was considerable evidence that the hippocampus was important for spatial learning and some evidence that it was also involved in duration discrimination. The article "Hippocampus, Time, and Memory" (Meck, Church, & Olton, 1984), however, was the first to isolate the effects of hippocampal damage on specific stages of temporal processing. In this review, to celebrate the 30th anniversary of Behavioral Neuroscience, we look back on factors that contributed to the long-lasting influence of this article. The major results were that a fimbria-fornix lesion (a) interferes with the ability to retain information in temporal working memory, and (b) distorts the content of temporal reference memory, but (c) did not decrease sensitivity to signal duration. This was the first lesion experiment in which the results were interpreted by a well-developed theory of behavior (scalar timing theory). It has led to extensive research on the role of the hippocampus in temporal processing by many investigators. The most important ones are the development of computational models with plausible neural mechanisms (such as the striatal beat-frequency model of interval timing), the use of multiple behavioral measures of timing, and empirical research on the neural mechanisms of timing and temporal memory using ensemble recording of neurons in prefrontal-striatal-hippocampal circuits.

Stimulus control in multiple temporal discriminations.

In multiple fixed interval (FI) schedules, rats are trained to discriminate different FIs that are signaled by different stimuli. After extensive training, the different stimuli often acquire control over performance, observed by an earlier increase in responding for stimuli that signal shorter FIs, as compared with stimuli that signal longer FIs. The order in which the different FIs are trained, either intermixed across cycles or in blocks of several cycles, may seem irrelevant given that average performance at asymptote may be similar. In this study, rats were trained in two procedures with multiple FIs presented intermixed within sessions or in blocks of one interval per session. Similar performance was observed at asymptote, but an inspection of early cycles in each session revealed that different stimuli acquired control over performance only when trained intermixed within each session. Although the stimuli reliably signaled the upcoming FI, when trained in successive blocks of 60 cycles, rats rapidly adjusted performance early in the sessions on the basis of the temporal aspects of the task, and not on the basis of the stimulus presented in the current cycle. These results are discussed in terms of overshadowing of the stimuli by temporal cues and in terms of conditions under which a stimulus acquires control over performance.

The importance of the reinforcer as a time marker.

Shifts in the psychometric function in the Free Operant Psychophysical Procedure (FOPP) have traditionally been explained by suggesting the pacemaker rate is proportional to the reinforcement rate (Behavioral Theory of Timing; BeT), or by direct associative competition between the two responses (Learning to Time; LeT). The application of these models assumes that the stimulus onset is the relevant time marker. Head-entries were reinforced in the second half of a stimulus (s1) and in the first half of a different stimulus (s2). During extinction, response times shifted earlier in s2 only, contrary to BeT. Competition between responses is an unlikely cause of the shift, contrary to LeT. We found a single-cycle correlation between the last food delivery and the time the rat stopped responding on s2. This correlation was also present in FOPP data. These results are consistent with the interpretation that the reinforcer, more than the stimulus onset, acted as the relevant time marker on this task.

The effect of stimulus discriminability on strategies for learning multiple temporal discriminations.

The goal was to identify training conditions under which temporal intervals that are signaled by different stimuli are memorized (i.e., the temporal behavior is readily shown to be under stimulus control). Undergraduate students were trained on three signaled temporal discriminations using a peak procedure. The intervals were trained in either blocks of trials or with trials intermixed within the session, and then they were given a transfer test with intermixed trials. There were two levels of stimulus discriminability, defined by the similarity of the stimuli. Most participants memorized the intervals when the discriminations were intermixed within the session, or were easy, but not when the discriminations occurred in blocks and were difficult. In the transfer tests, those participants trained in the difficult discrimination that occurred in blocks of trials typically continued to perform as they did during the last-trained interval, regardless of the stimulus presented. These results are better explained by a memory retrieval than a memory storage account.

A simultaneous temporal processing account of response rate.

The goal was to determine whether a signal (e.g., a click) at food availability affects timing behavior in rats. Twenty-four rats were trained on an appetitive lever-press procedure that varied on two dimensions: shape of the interreinforcer distribution (i.e., fixed-interval 60s or random-interval 60s) and number of signals (i.e., the presence or absence of a click at the time of reinforcer availability). The rats were randomly partitioned into one of four groups (each group had six rats): Fixed, Signaled-Fixed, Random, and Signaled-Random. The shape of the interreinforcer distribution affected the response pattern; the presence of the click affected response rate. These results provide support for a simultaneous temporal processing account of behavior.

The Hunter Laboratory of Psychology after 50 years.

After a half century of use by the Brown University Psychology Department, the Walter S. Hunter Laboratory of Psychology has been scheduled for renovation for another use, and a new building for the department is on the drawing board. Hunter Lab was specifically designed to house an experimental psychology department. Here we comment on the changes and adaptations necessary over the years as teaching and laboratory technology changed and as the department and the university grew larger, and we suggest considerations to others who are planning new or renovated buildings with similar purposes.

The generality of empirical and theoretical explanations of behavior.

For theoretical explanations of data, parameter values estimated from a single dependent measure from one procedure are used to predict alternative dependent measures from many procedures. Theoretical explanations were compared to empirical explanations of data in which known functions and principles were used to fit only selected dependent measures. The comparison focused on the ability of theoretical and empirical explanations to generalize across samples of the data, across dependent measures of behavior, and across different procedures. Rat and human data from fixed-interval and peak procedures, in which principles (e.g., scalar timing) are well known, were described and fit by a theory with independent modules for perception, memory, and decision. The theoretical approach consisted of fitting closed-form equations of the theory to response rate gradients calculated from the data, simulating responses using parameter values previously estimated, and comparing theoretical predictions with dependent measures not used to estimate parameters. Although the empirical and theoretical explanations provided similar fits to the response rate gradients that generalized across samples and had the same number of parameters, only the theoretical explanation generalized across procedures and dependent measures.

A comparison of responses and stimuli as time markers.

A rat's behavior, as well as a stimulus, may be a time marker. But do they lead to similar performance? Eight rats were trained on a 20-s DRL procedure in which head-entry responses were time markers, i.e., each head-entry response indicated that food would not be delivered for 20s. Concurrently, eight rats were trained on a control procedure in which light stimuli, yoked to the responses of a rat in the DRL procedure, were time markers, i.e., each light stimulus indicated that food would not be delivered for 20s. A comparison of performance between the two groups showed a lower response rate in the DRL procedure than in the yoked control procedure. However, similar response patterns between the two groups were observed, suggesting that rats anticipated the food similarly with a stimulus or a response as the time marker.

A modular theory of learning and performance.

We describe a theory to account for the acquisition and extinction of response rate (conditioning) and pattern (timing). This modular theory is a development of packet theory (Kirkpatrick, 2002; Kirkpatrick & Church, 2003) that adds a distinction between pattern and strength memories, as well as contributing closed-form equations. We describe the theory using equations related to a flow diagram and illustrate it by an application to an experiment with repeated acquisitions and extinctions of a multiple-cued-interval procedure using rats. The parameter estimates for the theory were based on a calibration sample from the data, and the predictions for different measures of performance on a validation sample from the same data (cross-validation). The theory's predictions were similar to predictions based on the reliability of the behavior.

Differences between simultaneous and blocked training detected by a transfer test.

Secondary data analysis was used to compare responding early on a transfer test from rats previously trained simultaneously or successively on multiple temporal discriminations for the same number of trials [Guilhardi, P., Church, R.M., 2005 a. Dynamics of temporal discrimination. Learn. Behav., 33, 399-416]. Three fixed intervals (30, 60, and 120 s) were signaled by three stimuli (light, noise, and clicker). Twelve rats were trained with the three stimulus-interval pairs intermixed on each experimental session (simultaneous condition); 12 other rats were trained in successive blocks of 10 sessions on each pair (blocked condition). Then, all rats had a transfer test in which all three stimulus-interval pairs were presented intermixed on each session. Rats in the simultaneous and blocked condition responded similarly during training, but differently during early stages of the transfer test. One possibility is that rats in the blocked condition were controlled by the previous interval, not by the current stimulus. These results challenge the usual assumptions from models of timing and conditioning that both simultaneous and blocked training produce learning of the associations between stimulus and interval in a multiple interval training task.

Shifts in the psychophysical function in rats.

The primary goal was to compare results from a free-operant procedure with pigeons [Machado, A., Guilhardi, P., 2000. Shifts in the psychometric function and their implications for models of timing. J. Exp. Anal. Behav. 74, 25-54, Experiment 2] with new results obtained with rats. The secondary goal was to compare the results of both experiments with dependent variables that were not used in the original publication. As in the original study with pigeons, rats were trained on a two-alternative free-operant psychophysical procedure in which left lever press responses were reinforced during the first and second quarters of a 60-s trial, and right lever press responses were reinforced during the third and fourth quarters of the trial. The quarters were reinforced according to four independent variable interval (VI) schedules of reinforcement. The VI duration was manipulated in each quarter, and shifts in the psychophysical functions that relate response rate with time since trial onset were measured. The results obtained with rats were consistent with those previously obtained with pigeons. In addition, results not originally reported were also consistent between rats and pigeons, and provided insights into the perception, memory, and decision processes in Scalar Expectancy Theory and Learning-to-Time Theory.