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. Author manuscript; available in PMC: 2014 Mar 4.
Published in final edited form as: Curr Biol. 2013 Feb 7;23(5):387–391. doi: 10.1016/j.cub.2013.01.023

Source memory in the rat

Jonathon D Crystal 1,*, Wesley T Alford 1, Wenyi Zhou 1, Andrea G Hohmann 1
PMCID: PMC3595394  NIHMSID: NIHMS435525  PMID: 23394830

Summary

Source memory is a representation of the origin (source) of information. When source information is bound together, it makes a memory episodic, allowing us to differentiate one event from another [1, 2]. Here we asked if rats remember the source of encoded information. Rats foraged for distinctive flavors of food that replenished (or failed to replenish) at its recently encountered location according to a source-information rule. To predict replenishment, rats needed to remember where they had encountered a preferred food type (chocolate) with self-generated (walking along a runway encountering chocolate) or experimenter-generated (placement of the rat at the chocolate site by an experimenter) cues. Three lines of evidence implicate the presence of source memory. First, rats selectively adjusted revisits to the chocolate location based on source information, under conditions in which familiarity of events could not produce successful performance. Second, source memory was dissociated from location memory by different decay rates. Third, temporary inactivation of the CA3 region of the hippocampus with lidocaine selectively eliminated source memory, suggesting that source memory is dependent upon an intact hippocampus. Development of an animal model of source memory may be valuable to probe the biological underpinnings of memory disorders marked by impairments in source memory.

Results and Discussion

People make judgments about the origin, or source, of information. Source memory refers to memories about the conditions under which a memory was acquired. Source information may include perceptual, contextual, temporal, affective, and other features that were present when the memory was formed. For example, if you search for your bike, you may initially be alarmed to discover the bike is missing, only to subsequently remember that today you arrived at work by car. In humans, source memory is involved in creating, remembering, and misremembering events. Source memory involves feature binding during encoding and access as well as evaluation processes during remembering. Consequently, episodic memory tasks in people (which focus on our memories for unique personal events) involve source monitoring because they recruit attributions about the origin of mental experiences [3, 4].

Rats have a detailed representation of earlier episodes. This includes recollection of information [5, 6], memory of what-where-and-when an earlier episode occurred [7–10], and the ability to retrieve information that was incidentally encoded and unexpectedly requested [11]. Thus, we asked if rats remember the source of encoded information, namely by discriminating between encountering food following self-generated (walking along a runway encountering a distinctive food type) and experimenter-generated (placement at the site of a distinctive food type by an experimenter) events.

Rats foraged daily for food in an 8-arm radial maze. Upon first exposure, rats obtained their first opportunity to eat regular rat chow and a preferred food type, chocolate. The first opportunity to eat (first helpings of food) provided an opportunity to study food locations. After a delay, rats were returned to the maze to test their memory of the earlier episode (i.e., the location of a distinctive food type encountered at first helpings). To obtain their second opportunity to eat chow (second helpings), the rats needed to avoid revisiting locations where they obtained their first helpings earlier that same day because old locations no longer provided chow. A second helping of chocolate could be obtained by revisiting the same location that provided chocolate earlier, but the chocolate location replenished (or failed to replenish) according to a source-information rule. Consequently, obtaining second helpings of chocolate required the rat to not only remember what food they encountered and where they found it, but also to remember how they came to acquire it. An experimenter placement of the rat occurred during its first helpings of food; the rat was placed in front of one food trough, with food dispensed after the animal entered the trough. The source of chocolate in first helpings (i.e., the study phase) determined if that location would replenish additional chocolate in second helpings (i.e., the test phase). If chocolate was obtained by placement feeding, then that location did not provide replenishment. By contrast, if chocolate was obtained by non-placement feeding (i.e., a self-generated event in which the rat walked along the runway to obtain chocolate), then chocolate replenished at that location in second helpings. If rats have source memory, then they should be able to revisit the chocolate location at second helpings at a high rate in the replenishment condition (and limit revisits in the non-replenish condition). By contrast, if rats do not have source memory, then they should revisit the chocolate location at equivalent rates in replenishment and non-replenishment conditions. An experimenter placement of the rat always occurred during their first helpings of food; the placement was either at a chow or at a chocolate location, which was randomly determined on each trial. The placement occurred equally often in each serial position of arm entries within first helpings, which was also randomly determined. Importantly, availability of chocolate during the second helpings depended on whether the rat obtained its first-helpings of chocolate via self-generated or experimenter-generated events. (See Supplemental Experimental Procedures available online.)

We asked whether rats selectively adjusted their revisits to the chocolate location based on their memories of the source of the encoded information (Experiment 1). Experiments 2–4 converge on the conclusion that source memory in rats is episodic in nature by controlling for other explanations. We also asked whether source and location memory decay at different rates (Experiment 3). Experiment 5 shows that a brain region thought to be critical for human episodic memory is also critical for this demonstration of source memory in rats.

Experiment 1

To determine whether rats can distinguish between memories of self-generated and experimenter-generated events, we replenished chocolate in second helpings only after the rats had a self-generated encounter with chocolate. Thus, the rats needed to remember where they found chocolate during first helpings and the source by which it was acquired (self or experimenter generated). When replenishment in second helpings was predicted by self-generated, but not experimenter-generated, events, rats preferentially revisited the chocolate location when it was about to replenish (t(15)=3.8, p<0.01; Figure 1A). Differential rates of revisiting chocolate-flavored locations were accomplished (in this and subsequent experiments) while rats accurately avoided revisits to depleted chow-flavored locations (see supplemental information Table S1 available online). The ability of rats to distinguish between memories of self-generated and experimenter-generated encounters of a distinctive food type is consistent with the hypothesis that rats have source memory.

Figure 1. Source memory is shown by a higher revisit rate to the replenishment than non-replenishment chocolate location.

Figure 1

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(A) Rats preferentially revisit the chocolate location when it is about to replenish in Experiment 1. Self-generated (replenish) and experimenter-generated (non-replenish) encounters with chocolate in study phases were presented in random order across sessions. * p < 0.01. (B) Rats preferentially revisit the chocolate location when it is about to replenish in a novel context in Experiment 2. Data come from one replenishment and one non-replenishment trial. * p < 0.01. (C) Source memory and location memory are dissociated by different decay rates across retention intervals of up to 7 days in Experiment 3. Source memory performance (indexed by more revisits to the replenishing chocolate location than to the non-replenishing chocolate location; left axis) is unaffected by retention-interval challenges of up to 2 days, whereas location memory (indexed by chow accuracy, right axis) completes its decay over this same time period. Source memory errors occur when the retention interval challenge is 7 days. At this time point, rats revisit the non-replenish chocolate location. These incorrect revisits are likely due to source memory failure because memory for the replenishing chocolate locations is intact at this time point. Rats encountered two chocolate locations per study phase, one self-generated and one experimenter-generated. (D). When experimenter-generated, but not self-generated, events predicted replenishment in second helpings (i.e., a reversal of the arrangement used in Experiments 1–3), rats preferentially revisited the chocolate location when it was about to replenish in Experiment 4. Because the rats revisited replenishing chocolate locations at which they had recently been handled by an experimenter, these findings rule out expression of a place preference (i.e., avoid aversive locations). + p < 0.0001. (A–D) Data show mean with one SEM; the probability of a revisit to the chocolate location was calculated from the first 4 (A–B) or 5 (C–D) choices in test phases.

Experiment 2

To determine whether rats used source memory flexibly rather than relying on memorized cues (e.g., handling, flavor, specific locations), we deprived the rats of a critical piece of information, namely the specific locations. We conducted a transfer test to a relatively novel room with different extramaze cues using the same rats. Importantly, because the rats did not have an opportunity to memorize the replenishment X encounter-contingencies at locations in the novel room, rats in the novel room could not rely on memorization when deprived of extra maze cues from the initial room used in training. Accordingly, if rats had relied on memorization in Experiment 1, then in the novel room they would visit the chocolate location at equivalent rates in replenishment and non-replenishment conditions (failure to transfer to the novel room). By contrast, if rats in Experiment 1 had learned a source-information rule, then in the novel room they would visit the chocolate location preferentially in the replenishment condition (successful transfer).

When first and second helpings occurred in a novel room, the rats preferentially revisited the chocolate location when it was about to replenish (t(15)=3.0, p<0.01; Figure 1B). It is unlikely that successful transfer of performance to the novel room is due to a failure to discriminate the two rooms because we independently verified that the two rooms are not substitutable; performance was severely disrupted when we conducted a study and test in different rooms. The fact that rats could differentiate between self-generated and experimenter generated encounters of food in a novel context is consistent with the hypothesis that rats monitor source information.

Experiment 3

Next, we asked whether source memory and general memory for spatial locations decay at different rates. Different forgetting rates would suggest that source and location memory are distinct and dissociable. In humans, memory systems can be dissociated by different forgetting rates [12–14]. Thus, we examined source memory and location memory (as indexed by chow accuracy) using a wide range of delays (retention intervals: 0–7 days) between first and second helpings of food; the delay in Experiment 1 was ~4 min. Prior to collecting data using long retention intervals, we trained the rats with two chocolate-baited locations in each first helping-phase, one of which was obtained as an experimenter-generated event and one as a self-generated event (with order and location randomly determined). This refinement allowed us to obtain both a replenishment and a non-replenishment condition each day, which more precisely matched the retention-interval challenges each day.

Revisits to the replenishment chocolate location (Figure 1C, squares) were uniformly high, even after a 7-day retention interval. By contrast, revisits to the non-replenishment chocolate location (Figure 1C, circles) were uniformly low for retention intervals of up to 2 days. The rats made source memory errors when the retention interval was 7 days by increasing revisits to the non-replenishment chocolate location. These are likely source-memory errors because they occur simultaneously without any loss of information about chocolate location. This observation is supported by the fact that the rats show retained accuracy in revisiting the replenishment chocolate location even after 7 days. This level of memory performance after a long retention interval in rats is remarkable and, to our knowledge, not documented in any other radial-maze experiment [15–17]. Source memory decay is further dissociated from location memory as shown by the different rates of forgetting at shorter retention-interval challenges; chow accuracy (Figure 1C, diamonds) rapidly decayed during the shortest retention intervals, whereas virtually no errors in source memory were observed at these retention intervals. Importantly, by the longest retention interval, we documented a change in chocolate revisit rates: Revisits to chocolate locations depended on both replenishment status and retention interval (interaction, F(3,36)=3.43, p<0.05); as expected revisits were also higher to replenishment than to non-replenishment (F(1,36)=124.79, p<0.0001) and increased across retention intervals (F(3,36)=4.71, p<0.01).

Experiment 4

Although a higher revisit rate to replenishment chocolate than to non-replenishment chocolate is consistent with source memory, an alternative hypothesis is that the rats were expressing a natural predisposition to avoid locations where aversive events recently occurred (i.e., handling by the experimenter). This possibility exists because in Experiments 1–3, non-replenishment was always at the location where the rat had recently been handled, raising the possibility that the experiment-generated events may have been mildly aversive. To test this non-source memory hypothesis, we put the predictions of source memory and place preference in conflict by reversing the replenishment contingencies. If the results of earlier experiments were dependent on a predisposition to avoid aversive locations [18], then the revisit rates should now be higher at the non-replenishment location. By contrast, if rats use source memory, then they should learn the new experimental contingency, in which case revisits should be higher at replenishment than non-replenishment chocolate locations.

When experimenter-generated, but not self-generated, events predicted replenishment in second helpings, rats preferentially revisited the chocolate location when it was about to replenish (t(12)=9.6, p<0.0001; Figure 1D). A preference for the replenishment chocolate location when replenishment occurred at either handled (Experiment 4) or non-handled (Experiments 1–3) locations is consistent with the hypothesis that rats have source memory.

Experiment 5

The hippocampus is posited to be a critical processing center in source memory [2, 19–22] and is implicated in episodic-like memory in non-human animals [23–25]. To test the hypothesis that our behavioral task requires source memory, we asked whether it was similarly hippocampal-dependent. Specifically, if our behavioral task requires source memory and that memory is hippocampal-dependent, then temporary inactivation of the hippocampus should impair the ability of rats to selectively revisit the replenishment chocolate location at a higher rate than the non-replenishment chocolate location. The CA3 region of the hippocampus is postulated to mediate short-term elements of episodic memory [11, 26–28]. Therefore, stainless-steel guide cannulae were implanted bilaterally above the CA3 region of the hippocampus to enable us to temporarily inactive this region using infusions of lidocaine.

Baseline source memory accuracy was reestablished after surgery (t(5)=7.9, p<0.001) demonstrating that surgical procedures alone did not disrupt performance. Next, to evaluate the impact of temporary inactivation of CA3, lidocaine or vehicle was infused before first helpings. The rats revisited the replenishment chocolate location at a higher rate than the non-replenishment chocolate location during baseline (Figure 2A). This difference was eliminated after lidocaine infusion (Figure 2A, t(5)=0.7, p>0.05). By contrast, after vehicle infusions, rats revisited the replenishment chocolate location at a higher rate than the non-replenishment location (t(5)=2.7, p<0.05), although the magnitude of this difference was attenuated relative to baseline (Figure 2A). These observations are supported by a significant interaction of condition X replenishment-status (F(2,10)=5.09, p<0.05); revisits rates were higher to the replenishment than non-replenishment condition (F(1,10)=11.50, p<0.05) but did not differ across conditions (F(2,10)=3.21, p>0.05). These results suggest that temporary inactivation of the hippocampus eliminated source memory discrimination. Histological analysis verified that the center of the injection sites was concentrated in CA3 (Figures 2B–2C). Performance did not differ in animals with clear bilateral placements in CA3 or placements where CA3 was targeted primarily unilaterally, and these animals were pooled for statistical analyses.

Figure 2. Temporary inactivation of CA3 before memory storage impaired accuracy in source memory performance.

Figure 2

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Source memory is indexed by a higher revisit rate to the replenishment chocolate location than to the non-replenishment chocolate location, as shown in baseline. This difference was eliminated after lidocaine infusion. By contrast, after vehicle infusions, rats revisited the replenishment chocolate location at a higher rate than the non-replenishment location, although the magnitude of this difference was attenuated relative to baseline. Data show mean with one SEM. The probability of a revisit to the chocolate location was calculated from the first 5 choices in test phases. Significant differences between bars connected by brackets are denoted by: × p < 0.05, + p < 0.0001. (B) Representative example of Nissl-stained section showing bilateral infusion sites targetting in the CA3 region of the hippocampus. Scale bar represents 500 µm. (C). Coronal diagrams showing locations relative to bregma of infusion sites for all rats. Note that bilateral infusions spared CA1 and the dentate gyrus.

Conclusions

Our findings suggest that rats monitor and remember the source of encoded information. We showed that source memory is dissociated from location memory and is hippocampal dependent, consistent with the hypothesis that source information is a feature of episodic memory. Judgments about the familiarity of recent events cannot explain preferential revisits to the replenishment location. First, chocolate replenishment was not predicted by the presence/absence of a recent placement because the placement always occurred during their first helpings of food. Second, chocolate replenishment could not be predicted by the recency of placement; placement occurred equally often in each serial position of arm entries within first helpings (randomly determined).

To determine if rats have source memory, we selected a source that included many salient features to distinguish self-generated and experimenter-generated events (e.g., tactile contact by an experimenter vs. floor contact, different spatial trajectories, levels of effort, and velocities, movements generated by self vs. an experimenter, etc.). Although it is not known which source characteristics the rats may have used, the replenishment or non-replenishment could not be predicted without source monitoring. The observation that rats possess source memory implies that source memory is evolutionarily quite old. Other approaches to study episodic memory in animals have focused on ecological problems faced by animals [29–31]. Source memory may be expected to confer survival benefit for the problems rodents face in social transmission of food preferences [32–34].

Source memory in our behavioral procedure is remarkably long lasting. Rats remember the location baited with chocolate for at least 7 days without any apparent decay. Not only is the ability to avoid the non-replenishment location intact without apparent decay for at least 2 days, but the rats also likely remembered the non-replenishment chocolate location after 7 days. By contrast, memory for chow locations, as defined by accuracy in avoiding revisits to chow locations, showed a decline that was complete after a 2-day retention interval. These results dissociate source memory from memory for location and flavor.

Errors of source memory occur in schizophrenia, posttraumatic stress disorder, depression, and Alzheimer's disease [2, 35]. Development of an animal model of source memory would be valuable for probing the neuroanatomical and molecular underpinnings of episodic-memory disorders. The ability to translate successfully from animals to humans will be improved by development of approaches that include modeling of the specific memory impairments observed in clinical populations [36], rather than general learning and memory assessments that are not specifically impaired. Moreover, understanding the functional organization of source memory will open opportunities to apply neurophysiological and genetic approaches to probe the neural and molecular underpinnings of memory disorders marked by impairments in source memory. These approaches can be used to understand changes in neuronal plasticity or neurotransmitter release that accompany source memory disorders in future research. These targeted approaches may ultimately yield therapeutic approaches that improve memory with limited side effects.

Supplementary Material

01

Highlights.

  • Rats monitor and remember the source of encoded information.

  • Source memory is dissociated from location memory.

  • Source memory survives very long retention-interval challenges (at least 2–7 days).

  • Source memory is dependent upon an intact hippocampus.

Acknowledgments

This work was supported by National Institute of Mental Health R01MH080052 to JDC.

Footnotes

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Supplemental Information

Supplemental Information includes Table S1 and Supplemental Experimental Procedures.

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