Trends in Cognitive Sciences
ReviewAnimal cognition and the rat olfactory system
Section snippets
Learning sets, olfaction and cognition
In his classic studies on ‘learning set’, Harlow 6 showed that, over time, monkeys presented with hundreds of simple, two-object visual discrimination tasks gradually made fewer errors, eventually achieving nearly errorless learning. They did this by learning something about the rules of the game. The first trial of each new task provided information about which choice would be rewarded; errorless learning was revealed by a monkey's correct responses on subsequent trials. Adopting the rule
Olfactory matching-to-sample
In a matching-to-sample test an animal is given a sample stimulus and then one or more comparison stimuli (see Fig. 1). It is a potentially powerful method for assessing non-spatial working memory, the relationship between inter-item interference and short-term memory and other aspects of cognitive behavior. The subject's task is to choose the comparison stimulus that is identical or most similar to the sample. A brief delay before presenting the comparison stimuli can be used to assess
Memory for odors
Otto and Eichenbaum 15 used the non-matching-to-sample procedure to examine short-term odor memory by imposing a delay between sequential presentations of odors. Under optimal conditions (use of many odors and a short delay between odor presentations) non-matching-to-sample accuracy was 90%; this declined to 75% with a 60 s delay (Fig. 3). Considerably better short-term memory was demonstrated using a procedure that essentially eliminated interitem interference 16: after being trained on a
Odor paired-associate learning
Other odor-cued tasks further extend our appreciation of what can only be viewed as ‘higher order’ learning by rats. To study paired-associate learning, rats were trained to sample two successively presented odors and were rewarded if they responded only to certain pairs (the paired-associate odors) 20. Responses after presentations of other odor pairs were not reinforced. There were eight pairs of associate odors and 112 types of trial containing other (non-reinforced) odor combinations. Rats
Odors, transitive patterning and transitive inference
In a conditional discrimination task in which subjects are rewarded if they respond to only one of two simultaneously presented stimuli using stimulus pairs A+/B−, B+/C− and C+/A− (where+and – indicate the reinforced and non-reinforced stimuli, respectively, in each odor pair), the correct choice is dependent upon the configuration of the stimuli and not on associations between individual stimuli and reinforcement. Dusek and Eichenbaum 21 found that, with odor cues, rats readily learned this
Neurobiology of olfactory cognitive behavior
Two classes of neurobiological investigation have emerged from the rodent studies described above: (1) those that have addressed the question of which olfactory pathways mediate different types of olfactory learning; and (2) those using odor learning to examine more general issues in cognitive neuroscience. An example of the first approach is a study on the role of olfactory pathways in the acquisition of an olfactory learning set 25. Rats with lesions of the mediodorsal thalamic nucleus (MD)
Conclusions
Comparative psychology is replete with demonstrations of small-brained animals, including insects, exhibiting complex associate learning and of larger-brained animals failing to learn similar tasks. As Dyer has observed, a major challenge in understanding animal cognition is to account for limitations in solving cognitive problems 35.
One such limitation may be unwittingly imposed when the experimenter uses stimulus cues that are inappropriate for efficient task performance. Most, and perhaps
Acknowledgements
I thank William Hodos and H. Philip Zeigler for their many useful suggestions and comments.
References (37)
The formation of learning-sets
Psychol. Rev.
(1949)Learning in vertebrates
- et al.
Olfactory learning set in two varieties of domestic rat
Psychol. Rep.
(1969) A method for establishing a five odorant identification confusion matrix task in rats
Physiol. Behav.
(1990)- Slotnick, B.M. and Schellinck, H. Methods in olfactory research with rodents. In Frontiers and Methods in Chemosenses...
Studies on retrograde and anterograde amnesia of olfactory memory after denervation of the hippocampus by entorhinal cortex lesions
Behav. Neural Biol.
(1986)Hippocampus, space, and relations
Behav. Brain Sci.
(1994)Spatial cognition: lessons from central-place foraging insects
What the rat's nose tells the rat's mouth: long delay aversion conditioning with aqueous odors/potentiation of taste by odors
Anim. Learning Behav.
(1997)- et al.
Olfactory and visual reversal learning in the pigeon
Chem. Senses
(1990)
Visualizing an olfactory sensory map
Cell
The enigma of olfactory learning
Trends Neurosci.
The enigma of olfactory learning revisited
Neuroscience
The central olfactory connections
J. Anat.
Dual olfactory representation in the rat thalamus: an anatomical and electrophysiological study
J. Comp. Neurol.
Evolutionary interpretation of neural and behavioral studies of living vertebrates
Proactive interference effects on short-term memory in rats: I. basic parameters and drug effects
Behav. Neurosci.
Effects of proactive interference on rats’ continuous non-matching-to-sample performance
Anim. Learning Behav.
Cited by (103)
Repeated reversals of concurrent olfactory discriminations in rats: A search for functional equivalence
2021, Behavioural ProcessesCitation Excerpt :Rats in the present study completed a greater number of reversals (M = 29.3, Range = 12–60) than those in Dube et al. (M = 4.6, Range = 0–10), even though the number of sessions completed was comparable. This considerable difference in the number of reversals completed is likely due to the use of olfactory stimuli (see Nigrosh et al., 1975; Slotnick, 2001). However, the present study still had a relatively low number of reversals completed compared to Vaughan (1988) and Kastak et al. (2001).
Directional tuning in the hippocampal formation of birds
2021, Current BiologyCitation Excerpt :Thus, the relative lack of place cells in our data and in data from other avian species remains a puzzle that is not likely to be accounted for by differences in behavior between birds and rodents, as here we recorded from birds freely roaming a square arena, similar in size and in recording conditions to many experiments in rats and mice that showed clear place cells and grid cells.50,87 Another possible explanation for the differences in spatial representation may stem from the fact that rodents strongly rely on somatosensation and olfaction,88,89 whereas quails and many other species of birds are primarily visual.90 Yet the findings of place cells in flying bats both when using vision and when using echolocation91 strongly suggest that, across species, the existence of place cells is not directly correlated with the dominant sensory modality of the species.
Rapidly training African giant pouched rats (Cricetomys ansorgei) with multiple targets for scent detection
2020, Behavioural ProcessesCitation Excerpt :In Part 1, we compared methods to rapidly retrain rats with novel targets revealing that training could be expedited by relaxing the false alarm criterion early on and by introducing targets with only novel S-s. Thus, these procedures were adopted for all rats during Part 2. Based on the results from Part 1 and previous research on learning set effects (e.g., Slotnick, 2001; Williams and Johnston, 2002; Wright et al., 2016), we hypothesized the rats would learn all three targets in significantly less time than was required for Part 1, while maintaining the ability to find all trained odor targets during maintenance tests interleaved with novel target training. Rats received sequential training on three novel S + odors (Fig. 8) following the Experimental Procedures described in Part 1, unless otherwise noted.
Fear paradigms: The times they are a-changin’
2018, Current Opinion in Behavioral SciencesSuccessive odor matching- and non-matching-to-sample in rats: A reversal design
2018, Behavioural ProcessesCitation Excerpt :The automated procedure increases experimental control by minimizing effects of handling and other distractions for the subject, as well as providing a more precise dependent measure. Slotnick and colleagues (see Slotnick, 2001 for a review) developed this procedure for rats and mice, demonstrating both discrimination and MTS with odor stimuli. In particular, Lu et al. (1993) used an automated procedure to test odor matching in rats, using successive conditional discrimination training (go, no-go).