The magic number 70 (plus or minus 20): Variables determining performance in the Rodent Odor Span Task

doi:10.1016/j.lmot.2013.03.001

Learning and Motivation

Volume 44, Issue 3, August 2013, Pages 143-158

https://doi.org/10.1016/j.lmot.2013.03.001 Get rights and content

Highlights

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We found high levels of accuracy in rats with up to 72 different stimuli in the odor span task (OST).
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This suggests that the OST is not measuring the same processes studied in human working memory.
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Span length was found to underestimate capacity in the OST.
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OST performance appears to involve a form of “what-when” or perhaps “how long ago” remembering.

Abstract

The olfactory span task (OST) uses an incrementing non-matching to sample procedure such that the number of stimuli to remember increases during the session. The number of consecutive correct responses (span length) and percent correct as a function of the memory load have been viewed as defining rodent working memory capacity limitations in several studies using the OST. However, the procedural parameters of the OST vary across experiments and their effects are not well understood. For example, in several studies, the number of stimuli to remember is confounded with the number of comparison stimuli displayed in the test arena. Experiment 1 addressed whether performance is influenced by the number of comparison choices available on any given trial (2, 5, 10) as well as the number of odor stimuli to remember during a session (12, 24, 36). Performance was most accurate when the number of stimuli to remember was low, as would be expected from a working memory interpretation of OST. However, accuracy was also affected by the number of comparison stimulus choices. High levels of accuracy were seen even with 36 odors, suggesting that the capacity for odor memory in rats was greater than suggested by previous research. Experiment 2 attempted to define this capacity by programming sessions with 36, 48 or 72 stimuli to remember in a group of rats that had previously received extensive OST training. Highly accurate performance (80% correct or better) was sustained throughout the session at even the greatest memory loads, arguing strongly against the notion that the OST models the limited capacity of human working memory. Experiment 3 explored the possibility that stimulus control in the OST is based on relative stimulus familiarity, rather than recognition of stimuli not yet presented during the current session. Number of odor cups visited increased with the number of comparisons in the arena, but rats rarely sampled all of the comparison odors before responding. However, on probe trials which included only stimuli that had been presented during the session, latency to respond and number of comparisons sampled was sharply increased. These data suggest that responding in the OST is determined not just by relative familiarity, but rather by a more specific “what-when” or perhaps “how long ago” form of stimulus control.

Section snippets

Subjects

Six male Holtzman (Sprague–Dawley) albino rats 90–120 days old at the beginning of the experiment served as subjects. Water was available ad lib., but access to food was restricted to maintain approximately 85% of free feeding weight. Subjects were individually housed and maintained on a 12:12 hr light/dark cycle.

Apparatus

The apparatus was a circular open-field arena (94 cm diameter) with 18 drilled holes (5 cm in diameter) arranged in two circular arrays on the floor (described previously in Galizio et

Experiment 2: Odor memory capacity in the OST

Experiment 2 was a further attempt to identify capacity limitations in the OST using rats with extensive OST experience in our laboratory. Ten rats tested in previous experiments assessing the effects of drugs on OST performances were studied here under successively longer span tasks (36, 48, and 72 sample stimuli to remember).

Experiment 3: Relative stimulus familiarity and OST performance

If performance in the OST involves relative judgments of familiarity, then it would seem necessary to sample each comparison stimulus in the array in order to guide response selection. Alternatively, responding could be based on a more absolute identification of odors that had not yet been presented within the session and thus would not require sampling of all stimuli in the array. Such a hypothesis would propose a more detailed type of stimulus control that included both the specific odor and

General discussion

The OST has generally been viewed as an assessment of rats’ working memory capacity, but the present results raise questions about this interpretation. In Experiment 1, we found that the number of comparison stimuli clearly influenced accuracy, a variable which is confounded with number of odors to remember in most previous OST experiments (Dudchenko et al., 2000, Rushforth et al., 2010, Rushforth et al., 2011, Turchi and Sarter, 2000, Young et al., 2007a, Young et al., 2007b, Young et al., 2008

Acknowledgements

This research was supported by DA029252 to Mark Galizio. The authors thank Melissa Deal, Andrew Hawkey, Kevin Jacobs, Heather Ward and Luke Watterson for assistance in data collection and analysis and Ashley Prichard for helpful comments on the manuscript.

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Trials after the distractor limit was reached always included one novel odor presented along with either 9, 4, or 1 distractor odors drawn randomly from those previously presented during the session. April et al. (2013) found that both span and overall percent correct were highest when the number of comparison stimuli was lowest (two) and that performance degraded somewhat as the number of distractors increased. There is wide variation in procedures across drug studies using the OST, and in many, the number of distractors has been permitted to increase with the memory load (e.g., Rushforth, Allison, Wonnacut, & Shoaib, 2010; Rushforth, Steckler, & Shoaib, 2011).
The rodent odor span task (OST) uses an incrementing non-matching to sample procedure in which a series of odors is presented and selection of the session-novel odor is reinforced. An OST is frequently used to test the effects of neurobiological variables on memory capacity as the number of odors to remember increases during the course of the session. In this regard, one important finding has been that NMDA receptor antagonists selectively impair OST performance at doses that spare accuracy on control tasks. However, in many versions of the odor span task the number of stimuli to remember is confounded with the number of distractor odors presented to the rat on each trial. The present study compared the effects of the NMDA antagonist dizocilpine when the number of choices was held constant at two (one novel odor—S+ and one previously presented distractor odor—S−) and when the number of choice stimuli was permitted to increase up to 10 (one S+ and 9 S−). Dizocilpine impaired OST accuracy at doses that had no effect on a reference memory control task in both 2-choice and 10-choice conditions; however, the dose-response function was shifted to the left in the 10-choice tests. The impairments produced by dizocilpine were exacerbated as the memory load increased in both 2- and 10-choice conditions. These findings support the hypothesis that NMDA antagonism reduces the number of stimuli that rats can remember accurately, but the interaction between the effective DZP dose and the number of distractors shows that drug effects on OST performances may involve attentional factors in addition to memory capacity. The findings also demonstrate that variations in number of OST distractors can be used to alter sensitivity of the task.
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Thus, we tested the effects of MIA on working memory capacity using the odor span task (OST) in rats (Dudchenko, Talpos, Young, & Baxter, 2013). The OST (Fig. 3A), developed by Dudchenko, Wood, and Eichenbaum (2000), is an incremental nonmatching-to-sample task in which rats or mice receive a food reward by choosing to dig in a bowl of sand with a novel scent (Davies, Greba, & Howland, 2013; Davies, Molder, Greba, & Howland, 2013; Dudchenko et al., 2000; Rushforth, Allison, Wonnacott, & Shoaib, 2010; Rushforth, Steckler, & Shoaib, 2011; Young et al., 2007) or by flipping scented lids (April, Bruce, & Galizio, 2013; Galizio, Deal, Hawkey, & April, 2013; MacQueen, Bullard, & Galizio, 2011). If the subject chooses the novel bowl, additional bowls are added one at a time with the previous bowl(s) repositioned on the platform until the subject chooses a previously rewarded bowl (recorded as an error).
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The magic number 70 (plus or minus 20): Variables determining performance in the Rodent Odor Span Task

Highlights

Abstract

Section snippets

Subjects

Apparatus

Experiment 2: Odor memory capacity in the OST

Experiment 3: Relative stimulus familiarity and OST performance

General discussion

Acknowledgements

Neuroscience & Biobehavioral Reviews

Learning and Motivation

Neurobiology of Learning and Memory

Learning and Motivation

Neuroscience Letters

European Neuropharmacology

Neuropharmacology

Animal models of amnesia

Matching- and non-matching-to-sample concept learning in rats using olfactory stimuli

Journal of the Experimental Analysis of Behavior

Matching-to-sample abstract-concept learning by pigeons

Journal of Experimental Psychology: Animal Behavior Processes

Exploring the limits of spatial memory in rats using very large mazes

Learning & Behavior

Forebrain NR2B overexpression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice

PLoS ONE

Animal models of working memory: A review of tasks that might be used in screening drug treatments for the memory impairments found in schizophrenia

Neuroscience & Biobehavioral Reviews