Hippocampal State-Dependent Behavioral Reflex to an Identical Sensory Input in Rats

We examined the local field potential of the hippocampus to monitor brain states during a conditional discrimination task, in order to elucidate the relationship between ongoing brain states and a conditioned motor reflex. Five 10-week-old Wistar/ST male rats underwent a serial feature positive conditional discrimination task in eyeblink conditioning using a preceding light stimulus as a conditional cue for reinforced trials. In this task, a 2-s light stimulus signaled that the following 350-ms tone (conditioned stimulus) was reinforced with a co-terminating 100-ms periorbital electrical shock. The interval between the end of conditional cue and the onset of the conditioned stimulus was 4±1 s. The conditioned stimulus was not reinforced when the light was not presented. Animals successfully utilized the light stimulus as a conditional cue to drive differential responses to the identical conditioned stimulus. We found that presentation of the conditional cue elicited hippocampal theta oscillations, which persisted during the interval of conditional cue and the conditioned stimulus. Moreover, expression of the conditioned response to the tone (conditioned stimulus) was correlated with the appearance of theta oscillations immediately before the conditioned stimulus. These data support hippocampal involvement in the network underlying a conditional discrimination task in eyeblink conditioning. They also suggest that the preceding hippocampal activity can determine information processing of the tone stimulus in the cerebellum and its associated circuits.     

Timescale dependence in a conditional temporal discrimination procedure

A conditional temporal discrimination procedure was used to test the scope and generality of the principle of timescale invariance (TSI). Rats were trained to make different temporal discriminations following four different auditory stimuli. After shorter stimuli, rats were reinforced for pressing the left lever, and after longer stimuli, rats were reinforced for pressing the right lever. The four auditory stimuli (a pure tone, pulsed tone, click, and white noise) were each presented for different pairs of durations (ranging from 2 vs. 8s to 32 vs. 128 s) within a single session, but the ratio between the shorter and longer duration was maintained constant at 1:4. With the shortest pair of durations (2 vs. 8s), rats showed a clear violation of TSI in both overall and relative response rates. Rats started responding later and persisted relatively longer on the left lever when the shorter duration was only 2s. We interpret these results with regards to a framing hypothesis, whereby TSI does not apply to relatively short durations when animals are simultaneously trained with wide ranges of intervals.     

Mediation of timing accuracy by operant behavior

We attempted to demonstrate that timing performance on a temporal discrimination would be enhanced if rats were required to fill a duration with behavior than when they were not required to respond. Six rats were trained to discriminate between a 3- and 9-s stimulus in a symbolic-matching-to-sample task. In two conditions, a tone was used to signal the sample, and in the other two conditions, a light was used to signal the sample. In two conditions, the rats were required to respond on a lever mounted on the rear wall of the experimental chamber before making their discriminative response to one of the two levers mounted on the front wall of the experimental chamber. In the other two conditions, the rear lever was not presented during sample presentation, and no response was required. Consistent with our predictions, timing performance was significantly better when a lever-response was required during sample presentation than when no response was required.     

Interstimulus interval as a discriminative stimulus: Evidence of the generality of a novel asymmetry in temporal discrimination learning

Three appetitive conditioning experiments with rats examined temporal discrimination learning within Pavlovian conditioning trials. In all experiments, the duration of a feature white noise stimulus signaled whether or not a subsequent 10-s target tone would be reinforced. In Experiment 1, the feature durations were 4 and 1 min. For one group of rats (Group 4+/1−), 4 min of noise signaled that the tone would be reinforced and 1 min of noise signaled that the tone would not be reinforced. A second group (Group 1+/4−) was trained with the reverse contingency. The results showed a clear asymmetry in temporal discrimination learning: rats trained with 4+/1− (Long+/Short−) learned the discrimination readily (responding more in the tone on reinforced than on nonreinforced trials), whereas rats trained with 1+/4− (Short+/Long) did not. In Experiment 2, the feature durations were shortened to 60 and 15 s. Due to strong excitatory conditioning of the 15-s feature, the reverse asymmetry was observed, with the Short+/Long− discrimination learned more readily than the Long+/Short− discrimination. However, Experiment 3 demonstrated that the original Long+/Short− advantage could be recovered while using 60− and 15-s feature durations if the excitatory conditioning of the feature was reduced by including nonreinforced feature trials. The results support previous research involving the timing of intertrial intervals and are consistent with the temporal elements hypothesis which holds that the passage of time is encoded as a series of hypothetical stimulus elements.     

Temporal discrimination learning by pigeons

Memory for time by animals appears to undergo a systematic shortening. This so-called choose-short effect can be seen in a conditional temporal discrimination when a delay is inserted between the sample and comparison stimuli. We have proposed that this temporal shortening may result from a procedural artifact in which the delay appears similar to the intertrial interval and thus, produces an inadvertent ambiguity or 'instructional failure'. When this ambiguity is avoided by distinguishing the intertrial interval from the delay, as well as the samples from the delay, the temporal shortening effect and other asymmetries often disappear. By avoiding artifacts that can lead to a misinterpretation of results, we may understand better how animals represent time. An alternative procedure for studying temporal discriminations is with the psychophysical bisection procedure in which following conditional discrimination training, intermediate durations are presented and the point of subjective equality is determined. Research using the bisection procedure has shown that pigeons represent temporal durations not only as their absolute value but also relative to durations from which they must be discriminated. Using this procedure, we have also found that time passes subjectively slower when animals are required to respond to the to-be-timed stimulus.     

Pigeons' timing of an arbitrary and a naturalistic auditory stimulus: tone versus cooing

Previous animal research has traditionally used arbitrary stimuli to investigate timing in a temporal bisection procedure. The current study compared the timing of the duration of an arbitrary, auditory stimulus (a 500-Hz tone) to the timing of the duration of a naturalistic, auditory stimulus (a pigeon cooing). In the first phase of this study, temporal perception was assessed by comparing psychophysical functions for the duration of tone and cooing signals. In the first set of tests, the point of subjective equality (PSE) was significantly lower for the tone than for the cooing stimulus, indicating that tones were judged longer than equivalent durations of cooing. In the second set of tests, gaps were introduced in the tone signal to match those present in the cooing signal, and no significant difference in the PSE for the tone or the cooing signal was found. A repetition of the testing conducted with gaps removed from the tone signal, failed to replicate the difference in the PSEs for the tone and cooing signals originally obtained. In the second phase of the study, memory for the duration of tone and cooing was examined, and a choose-long bias was found for both signals. Based on these results, it appears that, for pigeons, there may be no significant differences in either temporal perception or temporal memory for arbitrary, auditory signals and more complex, naturalistic, auditory signals.     

Effects of delays on human performance on a temporal discrimination procedure: evidence of a choose-short effect

Studies of temporal discrimination in non-human subjects have reliably shown a choose-short effect: higher matching accuracy on short-duration-sample trials than on long-duration-sample trials. This effect occurs as a function of increasing the delay between the onset of sample and comparison stimuli in a delayed matching-to-sample procedure. The present experiment investigated whether the choose-short effect could be demonstrated in human subjects under conditions which paralleled those used with non-human subjects. Subjects responded under a discrete-trial procedure in which they were required to push one of two buttons depending on the duration of a sample stimulus (a blue square on a computer monitor). Delays (0, 8, 16, and 32s) separated sample and comparison stimuli (two white boxes) and were tested both within and across several sessions. Intermediate durations (probe stimuli between 2 and 4s) were also presented. The addition of a delay between the sample and comparison stimuli produced a bias to judge intervals as short when the 8 and 32-s delays were tested across sessions and when the 0, 16, and 32-s delays were tested within the same session. Thus, the choose-short effect was produced in human subjects using the interval bisection procedure regardless of delay length.     

Differential acquisition of specific components of a classically conditioned arterial blood pressure response in rat

Presenting a 15-s pulsed tone, the conditional stimulus (CS(+)), followed by 0.5-s tail shock, to a well-trained rat causes a sudden, but transient, pressor response (C(1)). Blood pressure (BP) then drops before increasing again (C(2)). A steady tone of the same frequency never followed by a shock (a discriminative stimulus, or CS(-)) evokes a C(1) but not a C(2) response. Experiment 1 tested the hypothesis that this BP response pattern does not depend on the nature of the tone (i.e., pulsed vs. steady) used for CS(+) and CS(-). The tones were reversed from the traditional paradigm, above, in nine rats. The C(1) BP increase for a steady-tone CS(+) (+4.8 +/- 1.9 mmHg, mean change +/- SE) and a pulsed CS(-) (+2.9 +/- 1.3 mmHg) did not differ. Conversely, C(2) showed a clear discrimination (CS(+): +5.1 +/- 1.2 mmHg, CS(-): +0 .7 +/- 0.8 mmHg; P < 0.05). Experiment 2 tested the hypothesis that the C(1) and C(2) BP responses first appear at different times during training. On training day 1, five 15-s pulsed tones (CS(+)) were presented to each of 18 rats; the last tone was followed by a tail shock. Likewise, five steady CS(-) tones never followed by shock were given. Training continued for 2 more days, with each CS(+) followed by shock. At the end of day 2, CS(+) evoked a C(1) BP response (+3.9 +/- 0.9 mmHg) but no C(2) (+0.6 +/- 0.4 mmHg, not significant vs. pretone). By the end of day 3, CS(+) evoked a significant (vs. baseline) C(1) (+7.3 +/- 1.4 mmHg) and C(2) (+3.3 +/- 0.8 mmHg). Conversely, although CS(-) evoked a C(1) response (3.5 +/- 1.3 mmHg), there was no C(2) (+0.7 +/- 0.5 mmHg; not significant). We conclude that 1) C(1) and C(2) are acquired at different rates, 2) early in training C(1) is an orienting response evoked by both tones, and 3) C(2) is only acquired as an animal learns to associate the CS(+) tone with shock. This suggests that C(1) and C(2) are controlled by different processes in the brain.     

Attention to uninformative features expressed by pigeons in a duration matching-to-sample task

Pigeons were trained on a matching-to-sample task in which they had to respond to a different choice stimulus following the same durations (2 or 10 s) of two different signals. The duration signals consisted of a white light presented from the ceiling and a red light presented from the front wall. Subsequent test performance indicated that matching accuracy declined (1) when the set of choice stimuli following a duration signal differed from the set presented during training, and (2) when the color or location of the duration signal was changed from values used during training. These results are discussed in terms of attention to uninformative features of a visual stimulus.     

Species differences between rats and pigeons in choices with probabilistic and delayed reinforcers

An adjusting-delay procedure was used to study rats' choices with probabilistic and delayed reinforcers, and to compare them with previous results from pigeons. A left lever press led to a 5-s delay signaled by a light and a tone, followed by a food pellet on 50% of the trials. A right lever press led to an adjusting delay signaled by a light followed by a food pellet on 100% of the trials. In some conditions, the light and tone for the probabilistic reinforcer were present only on trials that delivered food. In other conditions, the light and tone were present on all trials that the left lever was chosen. Similar studies with pigeons [Mazur, J.E., 1989. Theories of probabilistic reinforcement. J. Exp. Anal. Behav. 51, 87-99; Mazur, J.E., 1991. Conditioned reinforcement and choice with delayed and uncertain primary reinforcers. J. Exp. Anal. Behav. 63, 139-150] found that choice of the probabilistic reinforcer increased dramatically when the delay-interval stimuli were omitted on no-food trials, but this study found no such effect with the rats. In other conditions, the probability of food was varied, and comparisons to previous studies with pigeons indicated that rats showed greater sensitivity to decreasing reinforcer probabilities. The results support the hypothesis that rats' choices in these situations depend on the total time between a choice response and a reinforcer, whereas pigeons' choices are strongly influenced by the presence of delay-interval stimuli.     

P300 from a single auditory stimulus

The P3(00) event-related brain potential (ERP) was elicited with auditory stimuli to compare 2 different discrimination tasks. The oddball paradigm presented both target and standard tones; the single-stimulus paradigm presented at target but no standard tone stimulus. Experiment 1 manipulated target stimulus probability (0.20, 0.50, 0.80) and produced highly similar P3 amplitude and latency results across probability levels for each paradigm. Experiment 2 factorially varied inter-stimulus interval (2 sec, 6 sec) and target stimulus probability (0.20, 0.80). P3 amplitude and latency were highly similar for both the oddball and single-stimulus procedures across all conditions.     

Reinstatement of a food-maintained operant produced by compounding discriminative stimuli

After a tone and a light were established as discriminative stimuli for food-reinforced responding in rats, presenting these stimuli simultaneously produced over three times as many responses as either the tone or light alone. Following this stimulus compounding test, responses during the tone and during the light were not reinforced (extinction) for 20 sessions, essentially eliminating responding. On stimulus compounding tests administered after the 10th and 20th extinction sessions, tone-plus-light continued to produce significantly more responding than the tone or light alone. The compound even produced responses when the individual stimuli no longer did. These results suggest that the simultaneous presentation of multiple extinguished discriminative stimuli may also contribute to the reinstatement of other positively-reinforced behaviors, such as drug taking.     

Rats’ (Rattus norvegicus) temporal discrimination of brief auditory stimuli: How does it compare with that of humans (Homo sapiens) and zebra finches (Taeniopygia guttata)?

The present study with rats replicated an experiment on the ability of zebra finches and humans to discriminate among brief auditory stimuli (see Weisman et al., 1999, Experiment 2). We trained rats with 27 3-kHz tones that varied in duration from 10 ms to 1420 ms. Reinforcement was contingent on responding (approaching the food well) to the nine medium-durations range tones (56-255 ms) but not to the nine short-durations range (10-46 ms) or long-durations range tones (309-1420 ms). Rats also received post-discrimination transfer tests with 2 kHz and 4 kHz tones that varied over the same durations as the 3 kHz tones. Rats acquired the temporal discrimination to a slightly lower level of accuracy than seen in finches or humans by Weisman et al. (1999). We tested for transfer of the temporal discrimination to find that rats, similar to humans (data from Weisman et al., 1999), transferred to untrained 2-kHz and 4-kHz tones at levels approaching accuracy to that achieved to the trained 3-kHz tone. By contrast, zebra finches (data from Weisman et al., 1999) failed to transfer their discrimination to the trained tone. We conclude that (a) rats discriminate among tone durations at least as well as they do among auditory frequencies and (b) rats like humans, but unlike finches, are insensitive to absolute pitch in their temporal discrimination.     

Interval bisection in spontaneously hypertensive rats

An interval bisection procedure was used to study time discrimination in spontaneously hypertensive rats (SHR), which have been proposed as an animal model for the attention deficit hyperactivity disorder (ADHD); Wistar Kyoto and Wistar rats were used as comparison groups. In this procedure, after subjects learn to make one response (S) following a short duration stimulus, and another (L) following a long duration stimulus, stimuli of intermediate durations are presented, and the percentage of L is calculated for each duration. A logistic function is fitted to these data, and different parameters that describe the time discrimination process are obtained. Four conditions, with different short and long durations (1-4, 2-8, 3-12, 4-16s) were used. The results indicate that time discrimination is not altered in SHR, given that no difference in any of the parameters obtained were significant. Given that temporal processing has been proposed as a fundamental factor in the development of the main symptoms of ADHD, and that deficits in time discrimination have been found in individuals with that disorder, the present results suggest the necessity of exploring time perception in SHR with other procedures and sensory modalities, in order to assess its validity as an animal model of ADHD.     

Stimulus change detection in phasic auditory units in the frog midbrain: frequency and ear specific adaptation

Neural adaptation, a reduction in the response to a maintained stimulus, is an important mechanism for detecting stimulus change. Contributing to change detection is the fact that adaptation is often stimulus specific: adaptation to a particular stimulus reduces excitability to a specific subset of stimuli, while the ability to respond to other stimuli is unaffected. Phasic cells (e.g., cells responding to stimulus onset) are good candidates for detecting the most rapid changes in natural auditory scenes, as they exhibit fast and complete adaptation to an initial stimulus presentation. We made recordings of single phasic auditory units in the frog midbrain to determine if adaptation was specific to stimulus frequency and ear of input. In response to an instantaneous frequency step in a tone, 28 % of phasic cells exhibited frequency specific adaptation based on a relative frequency change (delta-f = ±16 %). Frequency specific adaptation was not limited to frequency steps, however, as adaptation was also overcome during continuous frequency modulated stimuli and in response to spectral transients interrupting tones. The results suggest that adaptation is separated for peripheral (e.g., frequency) channels. This was tested directly using dichotic stimuli. In 45 % of binaural phasic units, adaptation was ear specific: adaptation to stimulation of one ear did not affect responses to stimulation of the other ear. Thus, adaptation exhibited specificity for stimulus frequency and lateralization at the level of the midbrain. This mechanism could be employed to detect rapid stimulus change within and between sound sources in complex acoustic environments.     

Strategy of auditory discrimination of scale in Java sparrows: they use both "imagery" and specific cues

We examined whether Java sparrows use imagery of auditory stimuli (imagery is a subject's mental representation of a stimulus by which the subject's behaviour may be governed under stimulus control even in the absence of the physical stimulus). Three types of ascending tone sequences were used. In the intact scale, sequence tones were played in ascending order. In the intact-masked scale, part of the sequence was masked by noise but the remaining scale was identical with the intact scale, whereas in the violated scale, the sequence could be heard as if tones were played slowly (Experiment 1) or quickly (Experiment 2). Subjects were divided into two groups: one group was trained to respond to the intact and intact-masked scales and to suppress response to the violation scale (imagery-positive group). The contingency was reversed for the other (violation-positive) group. In Experiment 1, all the birds acquired discrimination, but successful transfer to novel stimuli was observed only in the imagery-positive group, suggesting that the imagery of the tone sequence was used as a discriminative cue. Experiment 2 confirmed that the stimulus duration was a discriminative cue for both groups, suggesting that the birds also acquired discrimination using only specific cues.     

Modality and intermittency effects on time estimation

The modality of a stimulus and its intermittency affect time estimation. The present experiment explores the effect of a combination of modality and intermittency, and its implications for internal clock explanations. Twenty-four participants were tested on a temporal bisection task with durations of 200-800 ms. Durations were signaled by visual steady stimuli, auditory steady stimuli, visual flickering stimuli, and auditory clicks. Psychophysical functions and bisection points indicated that the durations of visual steady stimuli were classified as shorter and more variable than the durations signaled by the auditory stimuli (steady and clicks), and that the durations of the visual flickering stimuli were classified as longer than the durations signaled by the auditory stimuli (steady and clicks). An interpretation of the results is that there are different speeds for the internal clock, which are mediated by the perceptual features of the stimuli timed, such as differences in time of processing.     

Stimulus control over induction produced by upcoming food-pellet reinforcement

Research has demonstrated that rats increase their rate of lever pressing for sucrose reinforcement when food-pellet reinforcement will soon be available within the session. Recent results suggest that this increase occurs because stimuli in the session come to signal different levels of overall reinforcement. The present experiment tested this idea by having rats respond in two types of session. In one, they pressed lever A for 1% sucrose reinforcers in the first half of the session and lever B for food-pellet reinforcers in the second half (the opposing lever was retracted in the respective half). In the other, they pressed lever B for 1% sucrose reinforcers in the first half and lever A for 1% sucrose reinforcers in the second. Thus, the presence of lever A in the first half of the session was predictive of upcoming food-pellet reinforcement, but only lever B was ever used to obtain food pellets. Subjects responded at a higher rate on lever B in the first half of the session than on lever A, despite food-pellet reinforcement being unavailable in such sessions. Furthermore, they responded at a higher rate on lever B during probe sessions in which both levers were available. These results demonstrate that stimulus control over induction occurs when a stimulus becomes differentially associated with a heightened level of reinforcement. However, questions remain as to whether this association is Pavlovian or whether stimuli with "predictive value" may ever lead to induction.     

Effect of contingent auditory stimuli on concurrent schedule performance: an alternative punisher to electric shock

This study explored whether load auditory stimuli could be used as functional punishing stimuli in place of electric shock. Three experiments examined the effect of a loud auditory stimulus on rats’ responding maintained by a concurrent reinforcement schedule. In Experiment 1, overall response rate decreased when a concurrent 1.5 s tone presentation schedule was superimposed on the concurrent variable interval (VI) 180-s, VI 180-s reinforcement schedule. On the contrary, response rate increased when a click presentation schedule was added. In Experiment 2, the extent of the response suppression with a 1.5 s tone presentation varied as a function of the frequency of the reinforcement schedule maintaining responses; the leaner the schedule employed, the greater the response suppression. In Experiment 3, response suppression was observed to be inversely related to the duration of the tone; response facilitation was observed when a 3.0-s tone was used. In Experiments 1 and 2, a preference shift towards the alternative with richer reinforcement was observed when the tone schedule was added. In contrast, the preference shifted towards the leaner alternative when the click or longer duration stimulus was used. These results imply that both the type and duration of a loud auditory stimulus, as well as the reinforcement schedule maintaining responses, have a critical role in determining the effect of the stimuli on responding. They also suggest that a loud auditory stimulus can be used as a positive punisher in a choice situation for rats, when the duration of the tone is brief, and the reinforcement schedule maintaining responses is lean.     

Responding for sucrose and wheel-running reinforcement: effect of pre-running

Six male albino Wistar rats were placed in running wheels and exposed to a fixed interval 30-s schedule that produced either a drop of 15% sucrose solution or the opportunity to run for 15s as reinforcing consequences for lever pressing. Each reinforcer type was signaled by a different stimulus. To assess the effect of pre-running, animals were allowed to run for 1h prior to a session of responding for sucrose and running. Results showed that, after pre-running, response rates in the later segments of the 30-s schedule decreased in the presence of a wheel-running stimulus and increased in the presence of a sucrose stimulus. Wheel-running rates were not affected. Analysis of mean post-reinforcement pauses (PRP) broken down by transitions between successive reinforcers revealed that pre-running lengthened pausing in the presence of the stimulus signaling wheel running and shortened pauses in the presence of the stimulus signaling sucrose. No effect was observed on local response rates. Changes in pausing in the presence of stimuli signaling the two reinforcers were consistent with a decrease in the reinforcing efficacy of wheel running and an increase in the reinforcing efficacy of sucrose. Pre-running decreased motivation to respond for running, but increased motivation to work for food.