Pigeons may not use dual coding in the radial maze analog task

Using a radial maze analog task, T. R. Zentall, J. N. Steirn, and P. Jackson-Smith (1990) found evidence that when a delay was interpolated early in a trial, pigeons coded locations retrospectively, but when the delay was interpolated late in the trial, they coded locations prospectively (support for a dual coding hypothesis). In Experiment 1 of the present study, the authors replicated the original finding of dual coding. In Experiments 2 and 3, they used a 2-alternative test procedure that does not require the assumption that pigeons' choice criterion, which changes over the course of the trial, is the same on delay and control trials. Under these conditions, the pigeons no longer showed evidence for dual coding. Instead, there was some evidence that they showed prospective coding, but a more parsimonious account of the results may be that the delay produced a relatively constant decrement in performance at all points of delay interpolation. The original finding of dual coding by Zentall et al. might have been biased by more impulsive choices early in control trials but not in delay trials and by a more stringent choice criterion late in delay trials.     

Memory persistence of rats in a radial maze varies with training procedure

Different estimations of the time-course of spatial working memory have been reported. Some authors found working memory in the radial maze to be relatively long lasting, while others found more rapid exponential decay. In the present experiments it was attempted to account for the conflicting results by investigating the effects of different training procedures. Two types of training were examined under the same circumstances. A group of seven rats was given a series of delayed trials (5, 20, 60, and 120 min). Every delay was repeated at least four times and the delays were presented in an ascending order. The number of errors decreased at every delay except the last one (120 min), where error levels were constant (.50 errors/trial). The good performance was not based on use of intramaze cues or response chaining. In another group of seven rats the same delays were introduced in a quasi-random order and alternated with uninterrupted trials. The number of errors increased exponentially with the length of the delay. However, when this procedure was repeated, the number of errors decreased. These results suggest that training with delayed trials is a major factor to account for the differences in reports of memory persistence in the radial maze.     

Septal area lesions impair spatial working memory in homing pigeons (Columba livia)

The septo-hippocampal system in birds resembles that of mammals, motivating research into the function of the avian hippocampus while surprisingly little attention has been given to the septum. To investigate a possible role of the avian septum in memory, the effects of septal area lesions on a spatial working memory (SpWM) task was tested in homing pigeons. After preoperative training on an analogue eight-arm (feeders) radial maze, now sham-operated control and septal lesioned pigeons were then trained again on the same task of locating the four feeders on the test phase of a trial that were not baited during the sample phase of a trial. During the test phase of a working memory trial, septal lesioned pigeons, compared to both their own preoperative performance and the performance of the controls, required significantly more choices to locate the four baited feeders not baited during the sample phase of a trial, and they made significantly fewer correct responses to the now baited feeders on their first four choices. The results demonstrate that, like its mammalian counterpart, the avian septum plays an important role in SpWM, suggesting that at least some functional properties of the septum are evolutionarily conserved in birds and mammals.     

Gerbils in space: performance on the 17-arm radial maze.

In Experiment 1 six hungry gerbils received six trials per day on a 17-arm radial maze. During each trial the subjects were allowed to choose freely among the arms, each of which contained a food pellet, until each arm had been visited once or until eight minutes had elapsed. An error was recorded when the subject entered a previously visited arm. The gerbils quickly learned not to re-enter previously visited arms and generally made errors on fewer than 15% of entries, performance comparable to that of the rat and superior to that of other species tested in the radial arm maze. The intertrial-interval duration did not affect accuracy of arm choices during acquisition but did influence asymptotic accuracy. Accuracy did not change systematically over the six trials. A high proportion of arm entries were to nearby arms. Errors occurred most often towards the end of a trial. Odor cues were not important. When the number of trials per day was reduced from six to one, accuracy deteriorated slightly. In Experiment 2 neither the transposition of extramaze cues nor the placement of the maze in a different room had large disruptive effects on accuracy. In Experiment 3 the addition of three explicit intramaze brightness cues aided accuracy, perhaps by permitting the subjects to decompose the large maze into three smaller mazes, although there was no direct evidence that this was the case. Implications of a number of these results for models of spatial maze performance were discussed.     

Flexible memory processing by rats: use of prospective and retrospective information in the radial maze

Four experiments investigated the content of the memory used by rats in mediating retention intervals interpolated during performance in a 12-arm radial maze. The delay occurred following either the 2nd, 4th, 6th, 8th, or 10th choice. A 15-min delay had the greatest disruptive effect when interpolated in the middle of the choice sequence and less of an effect when it occurred either earlier or later. This pattern of results was obtained when either a free- or forced-choice procedure was used prior to the delay and regardless of whether postdelay testing consisted of completion of the maze or two-alternative forced-choice tests. Assuming that the disruptive effect of a delay is a function of memory load, this implies that the rats used information about previously visited arms (retrospective memory) following an earlier interpolated delay but information about anticipated choices (prospective memory) following a delay interpolated late in the choice sequence. There appeared to be a recency effect only in the early and middle delay conditions. This provides converging evidence for the dual-code hypothesis. No evidence for prospective memory was obtained following a 60-min delay.     

Release from proactive interference by experimental amnesia: electroconvulsive shock improves radial-arm maze performance in rats

Rats were trained in an eight-arm radial maze and tested using a proactive interference (PI) procedure. Each test trial consisted of forced choices of four randomly selected arms followed, after a 2-h delay, by free choices among all eight arms. Normally, rats chose correctly during the free choices by entering and retrieving food from the four arms not yet visited during the test trial. Occasionally, an interference trial preceded the test trial by 1.5 or 3 h; interference trials consisted of forced choices of another four arms and an immediate test. The presence of an interference trial lowered test-trial performance (PI). Electroconvulsive shock (ECS) administered immediately after the interference trial had no effect; i.e., PI was still observed. When ECS was administered at the midpoint of the 3-h intertrial interval, performance increased to control (no ECS, no PI) levels. Such release from PI, however, was not obtained, and test-trial performance remained inaccurate when ECS was delivered immediately after the forced choices of the test trial (either 1.5 or 3 h after the interference trial).     

Exponential decay of spatial memory of rats in a radial maze

The persistence of spatial memory of rats (n = 14) was investigated in an eight-arm radial maze. The animals were trained until the mean number of errors in the first eight choices was 0.2. The decay of performance with time was studied using delays of 5, 20, 60, 120, or 240 min between choices 4 and 5, during which the animal was removed from the apparatus. A delay of 60 min significantly impaired performance. The mean number of errors was not significantly different from the random choice level after a delay of 120 min. The increase in the number of errors with time was exponential. Comparison of the results with those of previous studies suggests that the nature of training may have effects on memory persistence in the radial maze.     

Remembrance of places lasts: Proactive inhibition and patterns of choice in rat spatial memory

A series of experiments was carried out to evaluate the notion that rats given a sequence of massed daily trials on the radial maze reset working memory at the end of each trial by deleting its contents. Although curves presented by D. S. Olton [Scientific American, 1977, 236, 82–98; In S. H. Hulse, H. Fowler, & W. K. Honig (Eds.), Cognitive processes in animal behavior, Hillsdale, N.J.: Erlbaum, 1978] show that rats return to errorless performance at the beginning of each trial after the first, the fact that accuracy falls less rapidly over choices on Trial 1 than on subsequent trials suggests a proactive inhibition (PI) effect. In Experiment 1, Olton's findings were replicated, and a PI effect was observed on Days 1–2 of testing. On Days 3–5, overall accuracy improved significantly and was associated with the development of a strong tendency for rats to enter adjacent alleys, which became particularly marked on the final trials of a day's testing. In order to prevent rats from achieving accurate performance by using an adjacent alleys pattern, a procedure was used in Experiment 2 which involved initial forced random choices followed by a retention test consisting of free choices. Repeated daily trials with this procedure yielded a significant PI effect, which was more marked at a 60-sec delay than at a 0-sec delay. Experiments 3 and 4 showed this PI effect to be robust and resistant to manipulations designed to produce release from PI. Both the PI effect and a strong tendency found in Experiment 1 for animals to avoid on the initial choices of Trial n those alleys most recently entered on Trial n?1 argue that rats do not reset working memory between trials.     

Dose- and delay-dependent working/episodic memory impairments following intraventricular administration of ethylcholine aziridinium ion (AF64A).

The present study examined the effects of intraventricular administration of the cholinergic neurotoxin ethylcholine aziridinium ion (AF64A) on performance of a radial arm maze task. Male Sprague-Dawley rats were trained to perform a delayed-nonmatch to sample radial arm maze task in which a 1-h delay was imposed between the fourth and fifth arm selections. Following acquisition, animals were injected bilaterally with AF64A (1.5 or 0.75 nmol/side) or artificial cerebrospinal fluid into the lateral cerebral ventricles and allowed 7 days to recover before behavioral testing resumed. Significant dose- and delay-dependent impairments in the radial maze performance were observed in AF64A-treated rats as evidenced by fewer correct choices following the delay and by more errors to complete the task. Long-term testing in this task revealed significant recovery of memory performance. These findings indicate dose-dependent impairments in memory following intraventricular administration of AF64A and spontaneous behavioral recovery following such insult.     

Development of reference and working spatial memory in preschool children

Three groups of preschool children (aged 18 to 28, 33 to 42, and 47 to 58 months) were given a radial search test similar to the radial arm maze used with nonhuman subjects. The children searched for chocolate sweets among 10 labeled locations in a room, 5 of which were baited with a sweet. Older children outperformed the intermediate group, who in turn outperformed the youngest group in requiring fewer choices to retrieve all of the sweets. Working memory and reference memory aspects of performance were then separated: Reference memory (restriction of choices to the baited subset) in older children was superior to that in the youngest group but not to that in the intermediate group. In terms of working memory (avoidance of repeat responses to already visited locations), the older group made fewer errors than the intermediate group, who, in turn, made fewer errors than the youngest group. We concluded that working and reference components of spatial memory in children may share common elements, perhaps the ability to recognize places as familiar, although reference memory may develop earlier than working memory.     

Control of pigeons' matching-to-sample performance by differential sample response requirements

Pigeons were trained on a matching-to-sample task in which sample hue and required sample-specific observing behavior provided redundant, relevant cues for correct choices. On trials that involved red and yellow hues as comparison stimuli, a fixed-ratio 16 schedule (FR 16) was required to illuminate the comparisons when the sample was red, and a differential-reinforcement-of-low-rates 3-sec schedule (DRL 3-sec) was required when the sample was yellow. On trials involving blue and green hues as comparison stimuli, an FR 16 schedule was required when the sample was blue and a DRL 3-sec schedule was required when the sample was green. For some pigeons, a 0-sec delay intervened between sample offset and comparison onset, whereas other pigeons experienced a random mixture of 0-sec and 2-sec delay trials. Test trial performance at 0-sec delay indicated that sample-specific behavior controlled choice performance considerably more than sample hue did. Test performance was independent of whether original training involved all 0-sec delay trials or a mixture of 0-sec and 2-sec delays. Sample-specific observing response requirements appear to facilitate pigeons' matching-to-sample performance by strengthening associations between the observing response and correct choice.     

Visuospatial working memory in school-aged children exposed in utero to cocaine.

OBJECTIVE: Among the neurocognitive impairments reported as associated with prenatal cocaine exposure, slower response time, and less efficient learning in school-aged children are common to findings from several laboratories. This study presents performance data on a spatial working memory task in 75 prenatally cocaine exposed (CE) and 55 nondrug-exposed (NDE) 8- to 10-year-old children. METHODS: Children were administered a novel neuropsychological measure of immediate- and short-term memory for visuospatial information, the Groton Maze Learning Test (GMLT), a computer-based hidden maze learning test that consists of a "timed chase test" (a simple measure of visuomotor speed), eight learning trials followed by a delayed recall trial after an 8-minute delay and a reverse learning trial. Performance is expressed as correct moves per second and number of errors per trial. RESULTS: Across all trials, the cocaine-exposed group showed significantly slower correct moves per second and made significantly more errors. There were no significant main effects for amounts of alcohol, tobacco, or marijuana exposure. After an 8-minute delay and compared to the eighth trial, cocaine-exposed children showed less consolidation in learning compared to nonexposed children. When asked to complete the maze in reverse, cocaine-exposed children showed a greater decrement in performance (decreased correct moves per second and increased errors) compared to the eighth learning trial. CONCLUSIONS: Children exposed in utero to cocaine exhibit a possible impairment in procedural learning and diminished efficiency in creating and accessing an internal spatial map to master the hidden maze.     

On the nonassociative nature of working memory

Rats were trained in an eight-arm radial maze in two experiments. A “fixed set” of four arms, randomly selected and sequenced, was assigned to each rat. The fixed set was always presented in the same order. Each training trial began with rewarded forced choices of the four arms in the fixed set. The trial concluded with a free-choice test among all eight arms after a delay of about 40 min; choices of the four arms not in the fixed set were rewarded. The degree to which the identities and order of the arms in the fixed set had been learned was assessed in a reversal test. The four arms that were not in the fixed set were presented at the beginning of the reversal test trial; after the usual delay a free-choice test was given, but choices of arms in the fixed set were rewarded. In both experiments, the rats showed no negative transfer in the reversal test. Moreover, sequences of postdelay choices during training varied across days, and the sequence of choices during the reversal test did not match the sequence of arms in the fixed set. The rats therefore learned little if anything about the identities and the order of arms in the fixed set in spite of the consistencies between trials and the maintenance of the fixed set in memory for 40 min within trials. The finding is congruent with the view of working memory as nonassociative.     

The effect of reinforcement probability on time discrimination in the midsession reversal task

We examined how biasing time perception affects choice in a midsession reversal task. Given a simultaneous discrimination between stimuli S1 and S2, with choices of S1 reinforced during the first, but not the second half of the trials, and choices of S2 reinforced during the second, but not the first half of the trials, pigeons show anticipation errors (premature choices of S2) and perseveration errors (belated choices of S1). This suggests that choice depends on timing processes, on predicting when the contingency reverses based on session duration. We exposed 7 pigeons to a midsession reversal task and manipulated the reinforcement rate on each half of the session. Compared to equal reinforcement rates on both halves of the session, when the reinforcement rate on the first half was lower than on the second half, performance showed more anticipation and less perseveration errors, and when the reinforcement rate on the first half was higher than on the second half, performance showed a remarkable reduction of both types of errors. These results suggest that choice depends on both time into the session and the outcome of previous trials. They also challenge current models of timing to integrate local effects.     

Effects of scopolamine on repeated acquisition of radial-arm maze performance by rats.

Rats repeatedly acquired the performance of selecting only the four baited arms in an automated eight-arm radial maze, with the arms containing food pellets randomly assigned prior to each session. During each 14-trial (trial: obtain all four pellets) daily session, the number of errors (selecting nonbaited arms or repeating arm selections) showed a within-session decline, and choice accuracy for the first four arm selections showed a positive acceleration across trials for all rats. An index-of-curvature statistic, calculated for total errors, was used to quantify both the within- and between-session improvement of performance. Scopolamine (0.03 to 0.3 mg/kg, ip), but not methylscopolamine (0.3 mg/kg), reduced the accuracy of the first four selections of each trial and increased total within-session errors for all rats. Session times also were increased by scopolamine. An examination of within-session accuracy showed only slight signs of improvement at the higher dosages of scopolamine. The results indicate that behavior in transition states maintained by reinforcement contingencies in the radial maze is similar to that maintained by extended chained schedules, despite the fact that some of the stimuli controlling behavior in the maze are absent at the moment behavior is emitted.     

Step changes in the intertrial interval in the midsession reversal task: Predicting pigeons' performance with the learning-to-time model

Our goal was to assess the role of timing in pigeons' performance in the midsession reversal task. In discrete-trial sessions, pigeons learned to discriminate between 2 stimuli, S1 and S2. Choices of S1 were reinforced only in the first half of the session and choices of S2 were reinforced only in the second half. Typically, pigeons choose S2 before the contingency reverses (anticipatory errors) and S1 after (perseverative errors), suggesting that they time the interval from the beginning of the session to the contingency reversal. To test this hypothesis, we exposed pigeons to a midsession reversal task and, depending on the group, either increased or decreased the ITI duration. We then contrasted the pigeons' performance with the predictions of the Learning-to-Time (LeT) model: In both conditions, preference was expected to reverse at the same time as in the previous sessions. When the ITI was doubled, pigeons' preference reversal occurred at half the trial number but at the same time as in the previous sessions. When the ITI was halved, pigeons' preference reversal occurred at a later trial but at an earlier time than in the previous sessions. Hence, pigeons' performance was only partially consistent with the predictions of LeT, suggesting that besides timing, other sources of control, such as the outcome of previous trials, seem to influence choice.     

Amphetamine disrupts both working and reference memories of rats trained in a radial maze

To assess the effects of amphetamine on working and reference memory rats were trained on a 12-arm radial maze with six arms baited and six arms unbaited until stable performance was achieved. Administration of 2.0 mg/kg d-amphetamine sulfate increased both working and reference memory errors, but only if a 5-min delay was imposed after three successful choices. With no delay this dose had no reliable effect on either working or reference memory. Lower doses (0.5 or 1.0 mg/kg) were ineffective even when a delay was imposed during the test. We suggest that amphetamine heightens arousal, which disrupts accurate retention when the rat's attention to the relevant cues is interrupted, as during a brief delay. Alternative explanations are discussed.     

Hamsters' (Mesocricetus auratus) memory in a radial maze analog: the role of spatial versus olfactory cues

The golden hamster's (Mesocricetus auratus) performance on radial maze tasks has not been studied a lot. Here we report the results of a spatial memory task that involved eight food stations equidistant from the center of a circular platform. Each of six male hamsters depleted the food stations along successive choices. After each choice and a 5-s retention delay, the hamster was brought back to the center of the platform for the next choice opportunity. When only one baited station was left, the platform was rotated to evaluate whether olfactory traces guided hamsters' choices. Results showed that despite the retention delay hamsters performed above chance in searching for food. The choice distributions observed during the rotation probes were consistent with spatial memory and could be explained without assuming guidance by olfactory cues. The radial maze analog we devised could be useful in furthering the study of spatial memory in hamsters.     

Damage to the retrosplenial cortex produces specific impairments in spatial working memory

Mounting evidence indicates that the retrosplenial cortex (RSP) has a critical role in spatial navigation. The goal of the present study was to characterize the specific nature of spatial memory deficits that are observed following damage to RSP. Rats with RSP lesions or sham lesions were first trained in a working memory task using an 8-arm radial arm maze. Rats were allowed 5 min to visit each arm and retrieve food pellets and a 5-s delay was imposed between arm choices. Consistent with previous research, rats with RSP damage committed more errors than controls. In particular, RSP-lesioned rats committed more errors of omission (failing to visit an arm of the maze), but there were no lesion effects on errors of commission (revisiting an arm). Neither group of rats exhibited a turn bias (i.e., always turning a certain direction when choosing an arm). At the end of the training phase of the experiment, both groups had reached asymptote and committed very few errors. In the subsequent test phase, a longer delay (30-s) was imposed during some sessions. Both control and RSP-lesioned rats continued to make few errors during sessions with the standard 5-s delay, but RSP-lesioned rats were impaired at the 30-s delay and committed more errors of commission, consistent with an increase in taxing spatial working memory.     

RISKY CHOICE IN PIGEONS AND HUMANS: A CROSS‐SPECIES COMPARISON

Pigeon and human subjects were given repeated choices between variable and adjusting delays to token reinforcement that titrated in relation to a subject's recent choice patterns. Indifference curves were generated under two different procedures: immediate exchange, in which a token earned during each trial was exchanged immediately for access to the terminal reinforcer (food for pigeons, video clips for humans), and delayed exchange, in which tokens accumulated and were exchanged after 11 trials. The former was designed as an analogue of procedures typically used with nonhuman subjects, the latter as an analogue to procedures typically used with human participants. Under both procedure types, different variable‐delay schedules were manipulated systematically across conditions in ways that altered the reinforcer immediacy of the risky option. Under immediate‐exchange conditions, both humans and pigeons consistently preferred the variable delay, and indifference points were generally ordered in relation to relative reinforcer immediacies. Such risk sensitivity was greatly reduced under delayed‐exchange conditions. Choice and trial‐initiation response latencies varied directly with indifference points, suggesting that local analyses may provide useful ancillary measures of reinforcer value. On the whole, the results indicate that modifying procedural features brings choices of pigeons and humans into better accord, and that human—nonhuman differences on risky choice procedures reported in the literature may be at least partly a product of procedural differences.