Chemical Senses Vol. 30 No. suppl 1 © Oxford University
Press 2005; all rights reserved
Odor-intensity Coding in the Anterior Piriform Cortex
1 Department of Physiology, Kanazawa Medical University, Uchinada, Ishikawa 920-0293, Japan and 2 Department of Oral and Maxillofacial Surgery, Kanazawa Medical University, Uchinada, Ishikawa 920-0293, Japan
Correspondence to be sent to: Norihiko Onoda, e-mail: n-onoda@ kanazawa-med.ac.jp
Key words: intrinsic signal, layer II, optical imaging, rostro-caudal gradient
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Introduction |
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The primary olfactory cortex is defined as the region that receives direct fiber projection from the olfactory bulb (OB). The piriform cortex (PC) is the largest structure in the olfactory cortex. However, no ‘point to point’ anatomical connection between the OB and PC has been found (Haberly, 1998
). In addition, no evidence that neurons with
similar odorant preferences are located in a cluster in the PC has been reported. A
recent study has demonstrated, however, that anterior PC neurons discriminate alkane
odorants based on carbon chain length (Wilson,
2001). On the other hand, genetic tracing studies in mice have indicated that
inputs from different odorant receptors are mapped onto overlapping clusters of neurons
in the PC (Zou et al.,
2001). It has been suggested, thus, that the coding for each odor is
spatially distributed in the PC (Haberly,
1998). Further, a recent mapping study of c-fos immunoreactivity in response
to odorants suggested odor-specific spatial patterns of activity within the anterior PC
(Illig and Haberly, 2003). It remains
unclear, however, whether there is any spatial organization or clustering of the PC
neurons with similar stimulus preferences.
Because the optical imaging method for detecting intrinsic signals has been used to
monitor neural activity in the sensory cortices (Bonhoeffer and Grinvald, 1993;
Yoshimura et al., 2004), high
resolution mapping of odor-induced activation is now possible. We explored the
organization of olfactory information processing in the anterior PC using optical imaging
and compared these data to unit activity.
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Methods |
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TopIntroductionMethodsResultsDiscussionAcknowledgementsReferences |
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Animal protocols used in this study complied with all pertinent institutional and Japanese Government regulations and every attempt was made to minimize the number of animals utilized. Twenty-nine and 11 guinea-pigs were used in the optical imaging and extracellular unit recording studies, respectively. Animals were anesthetized with Na-barbiturate. The skull overlying the anterior PC was thinned. The heart rate and rectal temperature were monitored continuously. The pulmonary rate and thorax movements were recorded. The animal’s heads were fixed on the stereotaxic frame (Onoda et al., 1984
) and tilted until the
camera field was as horizontal as possible. Intrinsic signals (absorption changes at 646
nm of light) in the anterior PC were recorded through silicone oil. The imaged area was
8.7 x 6.5 mm2 and contained 320 x 240 pixels. The intrinsic signal
images were recorded at 500 µm below the cortical surface. Amyl acetate (AA), n-butyl alcohol (butanol), butyraldehyde (butanal), diethyl ether (ether) and xylene were used as odor stimuli. Odorous vapor was delivered from the syringe by the push of each plunger, which was motor-driven and under the control of a pulse generator. Several odors were applied in order for 6 s at 5 min intervals to avoid habituation. Each trial consisted of a pairs of records with and without stimulation at 2.5 min intervals. For each record, 16 frames each with a 500 ms frame length were collected for 8 s.
Individual images from the 4th to the 15th frames with and without stimulation were
averaged. The average image without stimulation was subtracted from that with stimulation
and averaged across eight trials (a differential image). The statistically significant
pixels in signal intensity were calculated by a t-test (P < 0.05).
In this analysis, a Gaussian spatial filter was used (Tsunoda et al., 2001).
Extracellular single unit activity was recorded using glass microelectrodes from the rostral and caudal anterior PC regions. Each odor stimulus with different concentrations was tested at least four times to determine statistically the concentration threshold of the unit.
After optical and/or electrical recording sessions, a glass pipette containing
brilliant blue dye was inserted 
500 µm below the cortical surface into the
center of each active zone or of each unit-recording region and the dye was deposited.
The animal was perfused with 4% paraformaldehyde. Serial frontal sections at 40
µm thickness were analyzed histologically.
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Results |
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TopIntroductionMethodsResultsDiscussionAcknowledgementsReferences |
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Optical odor maps obtained from intrinsic signal imaging in the anterior PC
Odor-induced cortical active regions appeared in a narrow band beneath the rhinal
sulcus over the lateral olfactory tract (LOT), which was defined as the dorsal part of
the anterior PC (aPCd) in the rat (Haberly,
1998). Differential images demonstrated optical response to 1.0% AA
but no response to mineral oil. Focusing depths were changed vertically from 0 to 800
µm deep to the cortical surface. Average depth profiles (n = 6)
showed a great increase over 400 µm and a peak at 500 µm. Optical signals
disappeared at 800 µm. A histological section showed a marking spot (500
µm below the cortical surface) in layer II. These results indicate that active
regions in the aPCd primarily originate in layer II.
Optical maps of the aPCd in response to changes in concentrations of AA
AA at 0.01 and 0.03% evoked a small number of active spots in the most rostral aPCd region. AA at 0.1% induced several clusters of active spots in the narrow band. Application of 0.3% caused large clusters of strong activation in the AON and rostral aPCd and then small clusters of activation spread until it reached the caudal end of the LOT. Application of 1.0% AA generated a long and narrow band of strong activation. It appeared that increasing concentrations increased the number of active spots which spread into the extent of the caudal aPCd, suggesting a rostro-caudal gradient in activation.
Optical maps of different odorants in the aPCd
The lowest concentration odors generated a small number of active spots in the narrow band. Their locations of active spots in response to different odorants overlapped slightly. Medium concentration odors generated active spots as far as the caudal region. The highest concentration odors generated a large number of active spots in the whole aPCd. Locations of active spots obtained in response to different odorants with higher concentrations considerably overlapped. It appeared that increasing concentrations of various odors also showed a rostro-caudal gradient in activation in the aPCd.
A relation between a total area of cortical activation and odor concentrations
The relation between the total area and odor concentrations was examined. Total areas of the cortical activation were calculated from the number of the active spots. In general, the relation between the magnitude of the sensation felt and stimulus intensity is described by a power function. In log–log coordinates, the relation shows a straight line whose slope is the exponent in the power law. The average exponents of AA was 0.74 ± 0.14 (mean ± SE, n = 3). The exponents of butanal, ether and xylene were 0.53 ± 0.05 (n = 3), 0.57 ± 0.09 (n = 3) and 0.69 ± 0.11 (n = 3), respectively. It appeared that the relation between the total area of the cortical activation and concentrations might be described by a relatively linear power function within a certain concentration range.
Single-unit recordings of cortical neurons in response to changes in odor concentrations
The distribution of odor thresholds for cortical neurons recorded in rostral and caudal aPCd regions was examined. The mean concentration threshold for AA in the rostral units was 0.18 ± 0.06%, whereas that in the caudal ones was 1.62 ± 0.57% (mean ± SE). The mean thresholds in rostral and caudal units for AA were significantly different (t-test, P < 0.01). The mean threshold for xylene was 0.27 ± 0.14% and 1.45 ± 0.66% in rostral and caudal units, respectively. The difference between the mean thresholds for xylene in rostral and caudal units was also significant (t-test, P < 0.01). From these results, thus, neurons with lower concentration threshold in the aPCd were dominant in the rostral region, whereas neurons with higher concentration threshold were prominent in the caudal region, suggesting that cortical neurons have a rostro-caudal gradient in mean thresholds for odorants.
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Discussion |
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TopIntroductionMethodsResultsDiscussionAcknowledgementsReferences |
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In this study, optical images of intrinsic signals from the aPCd in response to odor stimulation are mapped. The results showed that response patterns of individual odorants were mapped onto spatially overlapping locations of neural activity in the long narrow band, corresponding to the aPCd. Further, lower concentrations elicited activation in the rostral region of the aPCd, whereas higher ones generated caudally spreading activation and increasing concentrations lead to increasing the total active areas. Data obtained from the depth profile and histological reconstruction demonstrated that the optical signals primarily originate in layer II. Works with tracers and with unit recordings have shown that the superficially situated tufted cells, which project mainly to rostral regions of the PC (Mori, 1987
), are
more responsive (Schneider and Scott,
1983). These tufted cells have shorter latencies and lower thresholds for
electrical stimulation of the olfactory nerve layer than mitral and internal tufted
cells, which project axons further caudally to the PC (Schneider and Scott, 1983;
Mori, 1987). Further, since a
rostro-caudal gradient in afferent versus association fibres has been described
(Haberly, 1998), the input is heaviest
in the rostral region of the PC. These findings imply that central olfactory connections
with a rostro-caudal gradient contribute into olfactory coding in the PC. The spatial
representation of odor concentration, therefore, might be due to the spatially organized
rostro-caudal gradient in axonal projections of bulbar output cells with the
rostro-caudal gradient in their thresholds and spatial differences in summed inputs from
bulbar cells would be occurred in the aPCd along a rostro-caudal axis. |
Acknowledgements |
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TopIntroductionMethodsResultsDiscussionAcknowledgementsReferences |
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This work was partially supported by Grants for Collaboration Research (C2001-1) from Kanazawa Medical University.
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References |
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TopIntroductionMethodsResultsDiscussionAcknowledgementsReferences |
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