Animal cognition and the rat olfactory system

doi:10.1016/S1364-6613(00)01625-9

Trends in Cognitive Sciences

Volume 5, Issue 5, 1 May 2001, Pages 216-222

https://doi.org/10.1016/S1364-6613(00)01625-9 Get rights and content

Abstract

Is smell a ‘primitive’ sense used primarily to guide biologically basic behaviors or might it be the sensory modality that allows some species to express complex learning and other forms of cognitive behavior? Historically, the olfactory system has been considered primitive and it is not surprising that, until recently, cognitive neuroscientists have ignored odor-guided behavior. However, we now know that the olfactory system has projections to the prefrontal cortex, entorhinal cortex and hippocampus, and that these connections support the acquisition of simple and higher-order instrumental tasks, as well as a robust memory for odors. It appears that animals with a well-developed sense of smell have the neural machinery to think with their noses.

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)

H.F. Harlow
The formation of learning-sets
Psychol. Rev.
(1949)
J.M. Warren
Learning in vertebrates
J.W. Jennings et al.
Olfactory learning set in two varieties of domestic rat
Psychol. Rep.
(1969)
S.L. Youngentob
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...
U. Staubli
Studies on retrograde and anterograde amnesia of olfactory memory after denervation of the hippocampus by entorhinal cortex lesions
Behav. Neural Biol.
(1986)
L. Nadel
Hippocampus, space, and relations
Behav. Brain Sci.
(1994)
F.C. Dyer
Spatial cognition: lessons from central-place foraging insects
B.M. Slotnick
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)
H. Duncan et al.
Olfactory and visual reversal learning in the pigeon
Chem. Senses
(1990)

P. Mobarts

Visualizing an olfactory sensory map

Cell

(1996)

I.C. Reid et al.

The enigma of olfactory learning

Trends Neurosci.

(1993)

B.M. Slotnick

The enigma of olfactory learning revisited

Neuroscience

(1994)

T.P.S. Powell

The central olfactory connections

J. Anat.

(1965)

J.L. Price et al.

Dual olfactory representation in the rat thalamus: an anatomical and electrophysiological study

J. Comp. Neurol.

(1983)

W. Hodos

Evolutionary interpretation of neural and behavioral studies of living vertebrates

S.B. Dunnett et al.

Proactive interference effects on short-term memory in rats: I. basic parameters and drug effects

Behav. Neurosci.

(1990)

M.J. Pontecorvo

Effects of proactive interference on rats’ continuous non-matching-to-sample performance

Anim. Learning Behav.

(1983)

Cited by (103)

Whole-brain studies of spontaneous behavior in head-fixed rats enabled by zero echo time MB-SWIFT fMRI
2022, NeuroImage
Understanding the link between the brain activity and behavior is a key challenge in modern neuroscience. Behavioral neuroscience, however, lacks tools to record whole-brain activity in complex behavioral settings. Here we demonstrate that a novel Multi-Band SWeep Imaging with Fourier Transformation (MB-SWIFT) functional magnetic resonance imaging (fMRI) approach enables whole-brain studies in spontaneously behaving head-fixed rats. First, we show anatomically relevant functional parcellation. Second, we show sensory, motor, exploration, and stress-related brain activity in relevant networks during corresponding spontaneous behavior. Third, we show odor-induced activation of olfactory system with high correlation between the fMRI and behavioral responses. We conclude that the applied methodology enables novel behavioral study designs in rodents focusing on tasks, cognition, emotions, physical exercise, and social interaction. Importantly, novel zero echo time and large bandwidth approaches, such as MB-SWIFT, can be applied for human behavioral studies, allowing more freedom as body movement is dramatically less restricting factor.
Repeated reversals of concurrent olfactory discriminations in rats: A search for functional equivalence
2021, Behavioural Processes
Citation 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).
Equivalence class formation has been difficult to demonstrate in nonhumans, but one method that has been successful is a simple discrimination procedure in which contingencies associated with two sets of arbitrary discriminative stimuli are repeatedly reversed. Pigeons and sea lions shift responding after encountering the newly-reversed contingency with only a few set members, showing evidence of functional equivalence. We used this strategy to determine whether similar findings would occur in rats using olfactory stimuli. Rats were trained to nose-poke in the presence of six stimuli arbitrarily designated as members of the positive set; responses to the six members of the negative set were not reinforced. When discriminative performance was established, contingencies associated with each set were reversed and re-reversed each time subjects met a performance criterion. All subjects successfully acquired the concurrent simple discriminations and were exposed to between 12 and 60 reversals, but none showed clear evidence of functional class formation until a final procedure in which the stimulus sets that had been in place were arbitrarily rearranged. Acquisition with these new stimulus sets was impaired, showing that class membership generated by the original stimulus sets interfered with learning the new ones, thus providing evidence of functional equivalence.
Directional tuning in the hippocampal formation of birds
2021, Current Biology
Citation 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.
Birds strongly rely on spatial memory and navigation. Therefore, it is of utmost interest to reveal how space is represented in the avian brain. Here we used tetrodes to record neurons from the hippocampal formation of Japanese quails—a ground-dwelling species—while the quails roamed in an open-field arena. Whereas spatially modulated cells (place cells, grid cells, border cells) were generally not encountered, the firing rate of about 12% of the neurons was unimodally and significantly modulated by the head azimuth—i.e., these were head-direction cells (HD cells). Typically, HD cells were maximally active at one preferred direction and minimally at the opposite null direction, with preferred directions spanning all 360° across the population. The preferred direction was independent of the animal’s position and speed and was stable during the recording session. The HD tuning was broader compared to that of HD cells in rodents, and most cells had non-zero baseline firing in all directions. However, similar to findings in rodents, the HD tuning usually rotated with the rotation of a salient visual cue in the arena. Thus, these findings support the existence of an allocentric HD representation in the quail hippocampal formation and provide the first demonstration of HD cells in birds.
Rapidly training African giant pouched rats (Cricetomys ansorgei) with multiple targets for scent detection
2020, Behavioural Processes
Citation 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.
Since 1997, APOPO, a non-profit organization based in Tanzania, has deployed African giant pouched rats (Cricetomys ansorgei) to detect landmines in post-conflict areas. More recent research suggests the pouched rats can also be trained to detect tuberculosis in human sputum samples. Despite proven success on both tasks, the potential impact of each rat is limited by the required training time and constraint to a single target odor. The aim of this project was to establish a technique to rapidly train pouched rats to detect multiple odor targets. Eight pouched rats were trained to detect five unrelated target odors in Experiment 1. In addition to training duration, we measured maintenance of all odor targets. In Experiment 2, we examined response persistence under conditions of extinction. Experiment 3 investigated whether refresher sessions before tests would maintain detection accuracy. The animals mastered all odor targets in significantly fewer sessions than APOPO’s operational rats require to master a single target odor. Importantly, rats demonstrated strong discrimination between targets and non-targets despite the potential for interference and forgetting, suggesting pouched rats can be trained to detect at least five targets simultaneously. These results have the potential to increase the impact of each detection rat by both decreasing training time and expanding operational versatility, e.g., a single rat could be trained to detect multiple diseases.
Fear paradigms: The times they are a-changin’
2018, Current Opinion in Behavioral Sciences
Fear is considered an integral part of the brain's defensive mechanism that evolved to protect animals and humans from predation and other ecological threats. Hence, it is logical to study fear from the perspective of antipredator-survival behaviors and circuits by sampling a range of threatening situations that organisms are likely to encounter in the wild. In the past several decades, however, mainstream fear research has focused on the importance of associative learning; that is, how animals become frightened of innocuous cues as consequences of their contingent pairing with aversive events. While significant discoveries have been made, contemporary fear models derived from learning studies are likely to provide only a partial picture of the brain's fear system because they cannot simulate the dynamic range of risky situations in nature that require various adaptive actions and decisions. This review considers two different approaches to study fear, grounded on behaviorism and ethology and examines their contributions in revealing the naturalistic workings of fear in guiding and shaping behavior as animals make real-world choices.
Successive odor matching- and non-matching-to-sample in rats: A reversal design
2018, Behavioural Processes
Citation 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).
There is a growing body of research on matching- and non-matching-to-sample (MTS, NMTS) relations with rats using olfactory stimuli; however, the specific characteristics of this relational control are unclear. In the current study we examine MTS and NMTS in rats with an automated olfactometer using a successive (go, no-go) procedure. Ten rats were trained to either match- or non-match-to-sample with common scents (apple, cinnamon, etc.) as olfactory stimuli. After matching or non-matching training with four odorants, rats were tested for transfer twice with four new odorants on each test. Most rats trained on MTS showed immediate transfer to new stimuli, and most rats trained on NMTS showed full transfer by the second set of new odors. After meeting criterion on the second transfer test, the contingencies were reversed with four new odor stimuli such that subjects trained on matching were shifted to non-matching and vice versa. Following these reversed contingencies, the effects of the original training persisted for many trials with new odorants. These data extend previous studies on same-different concept formation in rats, showing strong generalization requiring few exemplars. The critical role of olfactory stimuli is discussed.

View all citing articles on Scopus

View full text

Trends in Cognitive Sciences

ReviewAnimal cognition and the rat olfactory system

Abstract

Section snippets

Learning sets, olfaction and cognition

Olfactory matching-to-sample

Memory for odors

Odor paired-associate learning

Odors, transitive patterning and transitive inference

Neurobiology of olfactory cognitive behavior

Conclusions

Acknowledgements

Psychol. Rev.

Psychol. Rep.

Physiol. Behav.

Behav. Neural Biol.

Behav. Brain Sci.

Anim. Learning Behav.

Chem. Senses

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.

Review
Animal cognition and the rat olfactory system