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The Journal of Neuroscience, August 15, 2002, 22(16):6842-6845
BRIEF COMMUNICATION
Spontaneous versus Reinforced Olfactory Discriminations
Christiane
Linster1,
Brett A.
Johnson2,
Alix
Morse1,
Esther
Yue1, and
Michael
Leon2
1 Department of Neurobiology and Behavior, Cornell
University, Ithaca, New York 14853, and 2 Department of
Neurobiology and Behavior, University of California, Irvine, California
92697-4550
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ABSTRACT |
When the major response domains in the rat olfactory bulb that are
evoked by odorant enantiomers are compared, some of these odorant pairs
do not show significantly different activity patterns. Such pairs are
not spontaneously discriminated in a behavioral test. We show here that
even these similar odorants appear to evoke different activity patterns
when every data point in a glomerular activity array is compared. These
odorants also can be discriminated if they are subjected to
differential reinforcement. These data suggest that the method chosen
to assess olfactory discrimination will reveal different olfactory
capabilities of rats. The small differences in glomerular activity that
probably exist between any pair of odorants may serve as a basis for
odor discrimination when rats are differentially reinforced, thereby
establishing the remarkable limits of rat olfactory perception. At the
same time, the major differences in glomerular responses appear to serve as the normal basis for spontaneous odor discrimination.
Key words:
olfactory coding; enantiomers; optical isomers; odor
perception; neural representations; habituation; reinforcement
learning; olfactory bulb; glomeruli
| |
INTRODUCTION |
Part of understanding the olfactory
code requires one to be able to predict olfactory perceptions based on
neural representations. To test such predictions, it would be ideal to
use pairs of odorants that have a single difference in molecular
structure that would evoke a small difference in neural activity. One
could then determine if there was a perceptual difference between the
two odorants. A good candidate for such molecules are enantiomers,
which are pairs of odorants that differ only in their
stereoconfiguration. Some, but not all enantiomer pairs evoke different
olfactory perceptions (Friedman and Miller, 1971 ; Leitereg et al.,
1971; Laska and Teubner, 1999; Laska et al., 1999a,b; Laska and
Galizia, 2001; Rubin and Katz, 2001).
We previously reported that the rat olfactory glomerular responses
evoked by the enantiomers of carvone differed significantly, whereas
those evoked by enantiomers of limonene and terpinen-4-ol did not
(Linster et al., 2001). These data predicted that rats would
discriminate between the enantiomers of carvone but not between the
enantiomers of either limonene or terpinen-4-ol, and we observed
exactly that behavior pattern (Linster et al., 2001). Such data are of
interest because they show that neural responses can be used to predict
the perceptual qualities of odorants. These data also are of interest
because they are the first to indicate that rats fail to discriminate
between any two odorants and that the olfactory bulb response does not
differ between any two odorants.
However, we used a novel means to record the behavior of rats to access
their perceptions. Specifically, we habituated rats to the
( )-enantiomer and then determined whether the rats dishabituated to
the (+)-enantiomer or to other odorants (Linster et al., 2001). Dishabituation indicated to us that the rats regarded the test odor as
different from the original odor. This method elicits a spontaneous
response based on initial olfactory perception and thereby differs from
the more commonly used differential reinforcement of one odorant over
another to determine whether the odors can be discriminated after
training (Rubin and Katz, 2001; Slotnick, 2001).
We also used a novel means of comparing the olfactory bulb responses to
the odorants (Linster et al., 2001). Specifically, we compared the
maximal 2-DG uptake within previously identified glomerular response
domains, or modules, that have shared responses to odorants (Johnson
and Leon, 2000). This method differs from the more common qualitative
reports noting visible differences in glomerular responses to odorant
enantiomers in individual animals (Ma and Shepherd, 2000; Rubin and
Katz, 2001). One disadvantage of our previous analysis was that it
combined many individual measurements into a few response modules for a
simplified statistical comparison. Thus, the analysis may have
overlooked reliable differences involving areas considerably smaller
than the previously defined glomerular modules. We here show that if we
compare every data point in a glomerular activity array, rather than
focusing on modular analysis, we can measure differences in the
glomerular activity maps evoked by the enantiomers of limonene and
terpinen-4-ol. Given such potential differences, we predicted that rats
would learn to discriminate these odorants in a behavioral paradigm using differential reinforcement.
| |
MATERIALS AND METHODS |
Odorants. Enantiomers of limonene, along with
propanal and ethyl isovalerate, were purchased from Aldrich Flavors and
Fragrances (Milwaukee, WI). Enantiomers of carvone and terpinen-4-ol
were purchased from Fisher Scientific/Acros Organics (Pittsburgh, PA). Purities reported by the manufacturers were 98% for
(R)-()-carvone, 98% for
(S)-(+)-carvone, 95+% for
(S)-()-limonene, 97+% for
(R)-(+)-limonene, 97% for
(R)-()-terpinen-4-ol, 95% for
(S)-(+)-terpinen-4-ol, 98% for ethyl isovalerate,
and 97% for propanal.
Odorant exposures. The University of California, Irvine, and
Cornell University Animal Care and Use Committees approved all procedures involving animals. Groups of six male Wistar rat pups (postnatal days 19-22) received a subcutaneous injection of 2-DG (0.16 mCi/kg; Sigma, St. Louis, MO) immediately before a 45 min odorant
exposure. From each litter, two rats were used for a given enantiomer
pair. Limonene and terpinen-4-ol enantiomer exposures involved the same
litters, and a single additional rat from each of these litters was
exposed to the odorant vehicle as a control.
Odorant exposures for 2-DG uptake were conducted as reported previously
(Johnson et al., 1999). Odorants were volatilized by using high-purity
nitrogen gas bubbled through a 100 ml column of pure liquid in a gas
washing bottle at a flow rate of 250 ml/min. The nitrogen stream then
was mixed with ultra zero-grade air for a final flow rate of 2 l/min
(1:8 dilution of odorant vapor). After odorant exposure, rats
immediately were decapitated. Brains were frozen rapidly in
2-methylbutane at about 45°C and then stored at 70°C until sectioning.
Mapping of 2-DG uptake. Coronal sections (20-µm-thick)
were prepared with a cryostat. Every sixth section was taken for
autoradiography, and adjacent sections were stained with cresyl violet
as described previously (Johnson et al., 1998, 1999). The stained
sections were used both to direct sampling within the glomerular layer of the autoradiography section and to standardize the rostral-caudal position of sections in reference to anatomical landmarks (Johnson et
al., 1999). Discrete measurements of 2-DG uptake were directed by a set
of radial grids to give samples at ~120 µm intervals around each
section. Measurements were merged into standardized data arrays
covering the entire glomerular layer (Johnson et al., 1999). Arrays
from the two bulbs of each animal were averaged and then converted to
nanocuries per gram of 2-DG by using standards exposed to the
autoradiography films. Values in these arrays then were transformed
into z scores before statistical analyses (Johnson et al.,
1999).
Statistical analyses. Comparisons of patterns of 2-DG uptake
were made to examine small differences in 2-DG uptake pattern by
performing t tests at each of the 2500 locations of
z score-standardized arrays (Johnson et al., 1999). This
procedure is similar to standard analyses used in functional brain
mapping (Hess et al., 2000; Crespo-Facorro et al., 2001; Rubin and
Katz, 2001). We then constructed a rolled-out map of p
values to describe the most reliable differences in 2-DG uptake across
the glomerular layer. Any point within this data array is approximately
aligned with respect to its position within the bulb, but the absolute
size or position of any individual response within the glomerular layer
is not revealed by this array.
Olfactory discrimination. All behavioral training occurred
in a transparent Plexiglas chamber (51 × 38 × 25 cm)
divided with a sliding, opaque Plexiglas panel into a start area and a
test area (Linster and Hasselmo, 1999; Linster and Smith, 1999; Cleland et al., 2002). Ceramic bowls (9 cm diameter, 4.5 cm height) were used
to place the odorants and the reward together. At the beginning of each
daily training set, a cotton swab was saturated with a 0.1 ml
drop of diluted odorant. The cotton tip was covered with fine plastic
mesh and was then taped to the bottom of the bowl. The bowl then was
filled with bedding (Bed-O-Cobs 0.125 inch laboratory bedding). The
reward, a bit of sweetened cereal (Froot Loops; Kellogg's, Battle
Creek, MI), was buried in the bedding, which was replaced after every trial.
Shaping. Rats were first shaped to retrieve a reward by
digging through the bedding. At the beginning of each trial, the rat was placed in the start area. Two bowls were placed in the test area,
one containing both the cereal reward and the odor, the other
containing no reward and no odor. When the partition was removed, the
rat entered the test area and was allowed to dig in the bowls until it
retrieved the reward. During the first few trials, the reward was
placed on top of the scented bowl, but after several successful
retrievals, the reward was buried deeper and deeper into the bedding.
When the rat learned to dig to retrieve the reward, the bowls were
moved around in the test area to force the rat to use the odor to
locate the correct bowl. Shaping was considered to be complete when a
rat could successfully retrieve a reward that was deeply buried in the
scented bedding and when the rat would dig even in the absence of a reward.
Behavioral testing. We determined whether adult male Sprague
Dawley rats could learn to discriminate between pairs of isomers: (+)-
and ()-limonene, as well as (+)- and ()-terpinen-4-ol. For
comparison, we tested the ability of these rats to discriminate between
two pairs of control odorants, ethyl isovalerate (apple odor) and
propanal (unpleasant fruit odor), as well as (+)- and ()-carvone,
which we had shown previously to be easily discriminated by rats in our
habituation-dishabituation task. Because each odorant was only used
once, the same rats were used in all experiments. All four
discrimination tests were run in parallel, with the order randomized
for each rat.
During each trial, rats were presented with two bowls, each containing
one of the two enantiomers, but only one of the bowls reliably
containing the reward. The presentation of the reward was
counterbalanced between odorants. Each training set was comprised of 20 consecutive trials with the same two odorants. During each trial, we
recorded the bowl in which digging was first observed, but subjects
were left to dig in either bowl until the reward was retrieved. The
trial was terminated after 1 min if the rat did not dig at all. The
bedding in the bowls was exchanged after each trial. To ensure that the
rats were learning about the test odorants and not identifying the
cereal reward by its own smell, we presented the rewarded odorant
without the cereal reward on every fifth trial (probe trials). Shortly
after the rat registered a preference by digging in the bowl, the
reward was dropped onto the scented bedding to maintain the association
of the odorant with the reward. Rats that did not dig in either bowl on
more than one of these probe trials were excluded from the analysis.
Statistical analysis. Data analyses were performed using
SPSS statistical software on the average number of correct responses. During each experiment, some rats had to be excluded because they would
not perform the task on that particular day. A total of 11 rats were
tested on (+)- and ()-limonene, 10 rats on (+) and ()-terpinen-4-ol, 13 rats on (+)- and ()-carvone, and seven rats on
the control odorant comparison. After two-way ANOVA testing for
differences in correct responses to the rewarded odorant, pairwise
post hoc tests (Tukey's HSD) were performed to determine which odors induced significant differences in preferences. All tests
were two-tailed, and the  level was set at 0.05.
| |
RESULTS |
When z score-standardized arrays of 2-DG uptake evoked
by (+)-limonene were compared with those evoked by ()-limonene on an
individual position-by-position basis, a number of potentially significant t values were obtained (Fig.
1). The low p values often
were clustered together, a pattern unlikely to occur on the basis of
chance alone. These clusters were found in a scattered distribution
across the entire glomerular surface. Clusters of low p
values also were obtained in comparisons of patterns evoked by
(+)-terpinen-4-ol and ()-terpinen-4-ol. There were locations where
(+)-enantiomers evoked higher uptake than ()-enantiomers as well as
other areas in which uptake evoked by ()-enantiomers exceeded that
evoked by (+)-enantiomers. It should be noted that many of
these areas of apparently different activity were not obvious by simple
inspection of original activity maps, in contrast with our previously
reported differences in activity patterns evoked by carvone
enantiomers (Linster et al., 2001).
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Figure 1.
Rolled-out contour charts of the
entire glomerular layer indicate the distribution of p
values in two-tailed t tests performed between
enantiomer responses for both limonene and terpinen-4-ol at each
position within the arrays. Warm colors signify
locations where the ()-enantiomer evoked potentially greater uptake.
Cool colors indicate locations where uptake for the
(+)-enantiomer potentially exceeded that for the ()-enantiomer.
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Given these small apparent differences in glomerular activity patterns,
we considered the possibility that rats might respond differently to
these odorants if they were subjected to differential reinforcement.
Therefore, we reinforced their selection of one enantiomer over the
other with a sweetened food reward (Linster and Hasselmo, 1999).
Indeed, rats rapidly reached the learning criterion of 90% correct
responses for discrimination between both limonene enantiomers and
terpinen-4-ol enantiomers (Fig. 2). In
addition, they learned to discriminate between the enantiomers of
carvone and between two unrelated odorants. Although there were no
differences among groups in responses during the first five reinforced
discriminations, during trials 6-10, significant differences emerged
across the four-odorant set (F(3,37) = 10.191; p < 0.001). These differences arose between
the carvones and limonene (p < 0.001), between
the carvones and terpinen-4-ol (p < 0.02), as
well as between the two control odorants and both limonene (p < 0.001) and terpinen-4-ol
(p < 0.005). The number of correct responses to
the enantiomers of limonene and terpinen-4-ol were not significantly
different from each other, nor were those between the enantiomers of
carvone and the two control odorants. During trials 11-15, small
differences across odorant sets persisted (F(3,37) = 3.665; p < 0.021), and this difference arose solely between the enantiomers of
terpinen-4-ol and the control odors. There were no significant
differences observed during the last five trials in overall responses
to the four-odorant set. Thus, although rats eventually learned all
three enantiomer discriminations, they were slower to learn to
discriminate between the enantiomers of limonene or terpinen-4-ol than
between the enantiomers of carvone or between the two unrelated
odorants.
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Figure 2.
The mean percentage of correct responses to
odorants that had previously been rewarded, shown as a function of
trial number. Asterisks indicate a response that is
significantly different from the response to the control
odorants.
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DISCUSSION |
We previously showed that rats do not discriminate between (+)-
and ()-enantiomers of either limonene or terpinen-4-ol in a
spontaneous discrimination task (Linster et al., 2001). Here, we report
that rats subjected to differential reinforcement of the enantiomers
were able to discriminate the same odorant pairs. In our previous
modular analysis of glomerular activity patterns, the enantiomer pairs
of limonene and terpinen-4-ol appeared to evoke the same pattern of
activity (Linster et al., 2001). In contrast, a point-by-point
comparison of activity across the entire glomerular layer revealed
numerous, small areas of potential difference in the activity patterns
evoked by the same enantiomer pairs. Our data are consistent with the
idea that rats normally ignore small differences in glomerular activity
and use only the major differences in module responses to make
spontaneous perceptual judgments. Whereas small differences in
glomerular activity normally may be ignored, such small differences can
be used to make discriminations if the rats are subjected to the
motivational and experiential consequences of differential reinforcement.
Small differences in glomerular activation patterns could arise from
low-affinity responses to one odorant that are not present for the
other odorant. Small differences in glomerular activity also could
result if two odorants were differentially contaminated with other
odorants. At some level of analysis, all odorants are contaminated with
other odorants. In most studies on olfaction, where odorant purities
range from 95 to 99.9%, odorant impurities sum to equal 0.1-5% of
the total mass of the odorant preparation. Normal rats easily can learn
to identify a mixture of 0.01% cineole and 0.5% amyl acetate when
compared with 0.5% amyl acetate alone (Lu and Slotnick, 1998).
Therefore, it is clear that rats can perceive the levels of
contaminants that are found in odorants. One may predict that all
odorants (even different preparations of the same odorant) will
generate patterns of glomerular activity with at least small
differences from all other such patterns. Moreover, rats should be able
to use such differences to discriminate between all odorants, given
differential reinforcement. Indeed, we can find no report that shows
rats failing to discriminate between any two odorants when given
differential reinforcement. The major modular responses, however,
predict that some odorants will be judged to be similar and others
judged to be different when rats are asked to make a spontaneous
discrimination. In a world in which virtually all odorants are
perceived against a variable background of other odorants that are well
within the detection range of rats, categorical distinctions must
normally be accomplished by ignoring these contaminants. On the other
hand, differential reinforcement may allow rats to use minor glomerular responses, or any other differences they can detect, to accomplish the discrimination.
The broadly distributed pattern of small response differences across
much of the olfactory bulb glomerular layer also suggests that it may
be futile to lesion major foci in the olfactory bulb and predict that
even lesioned rats would be able to discriminate between two odorants
if they are reinforced for their choice (Lu and Slotnick, 1998). It
seems quite possible that even if all of the major foci were removed
(something that has yet to be accomplished), rats would still be able
to use small differences that are likely to persist after bulb damage
to support a reinforced discrimination.
In many ways, the use of habituation-dishabituation analyses may be
superior to the use of differential reinforcement in experiments attempting to understand the olfactory code. Not only does the procedure predict differences in modular response of odorant
enantiomers, it also can show a graded similarity in perception of
other closely related odorants, thereby allowing more extensive
correlations with neurobiological data. Indeed, correlating the
differences in perceptual response, as measured by the spontaneous
discrimination test, with the major differences in 2-DG patterns
generated by aliphatic acids of different carbon number (Johnson et
al., 1999) revealed a correlation coefficient of 0.92 (Cleland et al.,
2002). The high correlation of the major glomerular modules with
spontaneous discriminations suggests that this approach may be a
valuable tool for the understanding of the olfactory code. On the other hand, using differential reinforcement to assess the potential impact
of the small differences in glomerular responses may inform us about
the extraordinary olfactory abilities of rats.
| |
FOOTNOTES |
Received March 1, 2002; revised May 31, 2002; accepted June 6, 2002.
This work was funded by National Institute on Deafness and Other
Communication Disorders Grant DC03545 (M.L.).
Correspondence should be addressed to Christiane Linster, Department of
Neurobiology and Behavior, W249 Mudd Hall, Cornell University, Ithaca,
NY 14853. E-mail: CL243{at}cornell.edu.
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D. A. Wilson, A. R. Best, and R. M. Sullivan
Plasticity in the Olfactory System: Lessons for the Neurobiology of Memory
Neuroscientist,
December 1, 2004;
10(6):
513 - 524.
[Abstract]
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C. E. Reisenman, T. A. Christensen, W. Francke, and J. G. Hildebrand
Enantioselectivity of Projection Neurons Innervating Identified Olfactory Glomeruli
J. Neurosci.,
March 17, 2004;
24(11):
2602 - 2611.
[Abstract]
[Full Text]
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G. A. Wright and B. H. Smith
Different Thresholds for Detection and Discrimination of Odors in the Honey bee (Apis mellifera)
Chem Senses,
February 1, 2004;
29(2):
127 - 135.
[Abstract]
[Full Text]
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D. A. Wilson, M. L. Fletcher, and R. M. Sullivan
Acetylcholine and Olfactory Perceptual Learning
Learn. Mem.,
January 1, 2004;
11(1):
28 - 34.
[Abstract]
[Full Text]
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M. Ditzen, J.-F. Evers, and C. G. Galizia
Odor Similarity Does Not Influence the Time Needed for Odor Processing
Chem Senses,
November 1, 2003;
28(9):
781 - 789.
[Abstract]
[Full Text]
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D. A. Wilson
Rapid, Experience-Induced Enhancement in Odorant Discrimination by Anterior Piriform Cortex Neurons
J Neurophysiol,
July 1, 2003;
90(1):
65 - 72.
[Abstract]
[Full Text]
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TOP
ABSTRACT
INTRODUCTION
