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1Yale University School of Medicine, Department of Physiology, New Haven, Connecticut; 2University of Michigan, Department of Physics and Biophysics Research Division, Randall Laboratories, Ann Arbor, Michigan; and 3Marine Biological Laboratory, NeuroImaging Cluster, Woods Hole, Massachusetts
Submitted 30 March 2005; accepted in final form 15 June 2005
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ABSTRACT |
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INTRODUCTION |
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) discovered oscillations that appear in the mammalian vertebrate olfactory bulb during and after odorant presentations. Subsequently it has been shown that odorants evoke more or less complex oscillatory patterning across many animal species (e.g., Adrian 1950; Hughes and Mazurkowski 1962; Laurent and Naraghi 1994; MacLeod et al. 1998; Teyke and Gelperin 1999). However, the relevance and function of the oscillations is not clear. In other sensory systems, synchronous activity of neurons may be used by the brain as the mechanism underlying binding of different features of sensory information (Engel et al. 2001; Fries et al. 2001; Singer 1999; Von der Malsburg 1999; Whittington et al. 1996). Thus far, there are no results in vertebrates that have directly linked the olfactory bulb oscillations to a specific cognitive role. Although there is evidence that the oscillations have a role in the differentiation of similar odors in locusts (Stopfer et al. 1997) and slugs (Teyke and Gelperin 1999), they do not appear to have such a role in moths (Christensen et al. 2003), zebrafish (Friedrich et al. 2004), rats (Fletcher et al. 2005; Lowry et al. 2005), or rabbits (Adrian 1950; Di Prisco and Freeman 1985).
In earlier experiments, we used optical imaging with voltage-sensitive dyes to monitor the odor-evoked oscillations in the turtle olfactory bulb (Lam et al. 2000, 2003). We found that odorants evoke a slow depolarization and three independent oscillations in the turtle bulb. The three oscillations, rostral, middle, and caudal, differ in their amplitude, location, frequency, duration, and latency (e.g., Fig. 1A). In contrast to the results in locusts and slugs but similar to the result in moths, fish, rats, and rabbits, the oscillations in the turtle appear to be independent of odor quality or concentration (over a substantial range of concentrations) (Lam et al. 2000, 2003).
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METHODS |
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The design of the olfactometer was copied from Kauer and Moulton (1974) with minor modifications (Lam et al. 2000). Cleaned and desiccated carrier air and laboratory air saturated with odorant vapor were injected into and mixed in the inner tube of a double-barrel odor applicator. The flow rate of the carrier air was set to 300 ml/min. The outer tube of the applicator was normally under suction at 1,500 ml/min to ensure that odorant does not leave the tube between the odorant applications. At a command pulse to a solenoid valve (South Bend Controls, South Bend, IN), this suction was turned off to release a pulse of diluted odorant. An additional solenoid valve was placed between the syringe pump and the odorant containers to allow for fast switching between the odorants during a trial. To draw the odorant through the nasal cavity, suction (300 ml/min) through tubing inserted into the pharyngeal opening (see following text) was activated 500–1,000 ms before the odorant presentation and was maintained for 15 s after the second odorant presentation. In a few animals, drawing room air alone through the nose elicited an oscillation of intermediate frequency (8 Hz) and very long duration (Lam et al. 2000). Recordings with this oscillation were not included in this paper. The minimum interval between trials was 60 s. We used 1- or 2-s odor pulses. Previous results indicated that longer odorant pulses did not substantially affect the amplitude or duration of the oscillatory response (Y.-W. Lam, L. B. Cohen, M. Wachowiak, and M. Zochowski, unpublished observations).
Surgery and staining
Oscillations were measured in experiments on 28 box turtles, Terepene sp. Not all animals were used for the statistical calculations either because too few trials were recorded or because only one or two of the three oscillations had signal-to-noise ratios large enough to make meaningful measurements. Experiments with signal-to-noise ratios of less than three were not analyzed. The composition of turtle saline that was used for dye dilution as well as washing the bulb during the experiment is as follows (in mM): 96.5 NaCl, 2.6 KCl, 2.0 MgCl2, 31.5 NaHCO3, 4.0 CaCl2, and 10 dextrose (all from Sigma, St. Louis, MO). The saline was bubbled with 95% O2-5% CO2 resulting in a pH of 7.0–7.2.
The turtles were partially immobilized with d-tubocurarine (1.5 mg/kg, Sigma) and anesthetized by placing them on ice 2 h before as well as during the surgery. Local anesthetic (1% bupivicane, Sigma) was applied around the location of the craniotomy. A segment of polyethylene tubing (2 mm OD, 1 mm ID) was inserted into the outlet of the nasal cavity in the roof of the mouth and fixed in place by Krazy Glue and epoxy. The dorsal surface of both olfactory bulbs was exposed by craniotomy of the overlying scull and removal of the dura and arachnoid matter.
VOLTAGE-SENSITIVE DYE MEASUREMENTS.
We used the fluorescent styryl dye, RH414 (Grinvald et al. 1994) (Molecular Probes, Eugene, OR; concentration 0.05–0.1 mg/ml in saline). The dye was applied directly to the exposed bulbs for 60 min; the solution was replaced every 15 min. After staining, the remaining dye solution was removed, and 2% agarose (Sigma) was placed on top of the bulbs. A coverslip was placed on top of the agarose to ensure a flat imaging surface. All of the results come from single-trial measurements; signal averaging could not be used because the oscillations were not precisely time-linked to the odorant pulse.
CALCIUM DYE MEASUREMENTS. Olfactory receptor neurons were labeled with Calcium Green-1 dextran, 10 kD molecular weight (Molecular Probes) by injecting 20 µl of 2% dye solution dissolved in 0.1 M NaCl plus 0.5% Triton-X 100 into each naris. After staining, the animals were held at room temperature for 5–18 days before the measurements. Similar surgical procedures were performed except that the bone covering the olfactory bulb was only thinned and the imaging was performed through the thinned bone.
Before starting the measurements the turtle was kept at room temperature for 1 h.
The upper jaw was clamped to a metal bar with a plastic strap to stabilize the head during the optical recordings. The turtles were not anesthetized during the recordings. All experimental procedures were approved by the Yale University and the Marine Biological Laboratory Institutional Animal Care and Use Committees.
Imaging
For the voltage-sensitive dye measurements, the preparation was illuminated using a 100-W tungsten bulb. The light was heat filtered and passed through a 520 ± 45 nm incident light filter. The fluorescence emission >610 nm was collected via a Macroscope (x4 magnification, RedShirtImaging, LLC, Fairfield, CT) onto a 464-element photodiode array (NeuroPDA, RedShirtImaging). Each pixel of the photodiode received light from an area of the image plane of 
170 µm2. The average recorded light intensity is 108 photons · ms–1 · pixel–1; the amplifier filtering was set to 0.5–125 Hz. For the Calcium dye measurements, the preparation was illuminated with the same illumination source and a 480 ± 25 nm incident light filter. The fluorescence emission above 530 nm was collected and measured with the photodiode array. The estimated recorded light intensity is 5 x 107 photons/ms/pixel; the same amplifier filtering was used.
Data analysis
NeuroPlex software (RedShirtImaging) was used for much of the data analysis and display. We applied digital filtering using high and low-pass Gaussian (5–30 Hz) filters. The results in Figs. 1, 2, 4, and 6 come from the outputs of individual pixels or the average of 10–20 neighboring pixels in the photodiode array.
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). Without this improved spatial resolution it would have been difficult to determine that repeated presentations had differential effects on the three oscillations. In almost all preparations, we found pixels in rostral locations that had only the rostral oscillation. However, in only about half of the preparations could we find locations that had isolated middle and/or caudal oscillations. In the remaining animals, the middle and caudal oscillations overlapped in location. In these instances, the two oscillations were identified by their latency, frequency, duration, and response to repeated stimulus presentation.
CHANGES IN POWER OF THE OBSERVED OSCILLATIONS IN REPEATED PRESENTATIONS.
Two data fragments of the same duration (1 for each presentation) containing one of the three observed oscillations were chosen. The power spectrum was calculated and the relative change of the power, C, at the peak frequency of the oscillation was calculated according to equation
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where P1 and P2 are the powers of the same oscillation after the first and second odorant presentation, respectively. The measure C takes values between –1 and 1. An increased oscillation will yield positive values of C, whereas a decrease will result in negative values. This measure was used because it avoids infinite values that would occur if we calculated simple percentage changes from results like those illustrated in Fig. 4. In the instances where the caudal oscillation appeared only as a high-frequency oscillation, we calculated the change of power based on the power of high-frequency peak on the second presentation. The total number of trials observed (T) is indicated in the brackets in Table 1 and Fig. 3.
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RESULTS |
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; Youngentob et al. 1987). The aim of the present study was to elucidate possible roles of the odor evoked oscillations in the olfactory bulb of the turtle by determining whether changes in oscillations occur in response to multiple odorant presentations. We used odorant presentations of 1 or 2 s, short compared with the respiratory rate of resting box turtles which ranges from 0.01 to 0.2 Hz (Landberg et al. 2003). In other experiments, similar oscillations were measured in response to 0.5-s odorant presentations (data not shown).
We made voltage-sensitive dye measurements of odor-evoked responses in the turtle bulb using a 464-element photodiode array camera. Changes in dye fluorescence provide a fast, presumably linear, measure of the population averaged membrane potential changes (Grinvald et al. 1988; Ross et al. 1977; Zochowski et al. 2000) of the neural membranes imaged onto each pixel. In the experiments reported here, we presented trains of two or more stimuli with an odorant concentration between 0.3 and 10% of saturation and an inter-stimulus interval between 2 and 10 s.
The oscillatory response to the second presentation of the same odorant changed dramatically. Figure 1, A and B, illustrates a typical result: in response to the second odor presentation, the rostral oscillation was greatly diminished and often undetectable; the size of the caudal oscillation was also decreased substantially, and, in addition, its frequency in response to the second odorant pulse was twice that found in the first response; and finally the size and duration of the middle oscillation (the oscillatory response with the shortest latency) was increased. The responses to the third and subsequent odorant stimuli were similar to the response to the second stimulus.
The three oscillations occur over relatively large areas (1 mm2) of the turtle bulb (Lam et al. 2000, 2003). While Figs. 1, 2, and 4 illustrate results from individual pixels in the photodiode array; the results shown for the effects of repeated odorant presentation were similar for all pixels exhibiting an oscillation.
The time course of the change in oscillatory power (C; see METHODS) as a function of interstimulus interval (ISI) is shown in Fig. 5. The time course of the increase in the middle oscillation to identical odorants is similar to the time course of the decline when different odorants were presented. The effect of the first stimulus on the succeeding response declined substantially for all three oscillations when the ISI was 12 s. When much longer interstimulus intervals (>30 s) were used, the response to the second odorant presentation was similar to the response to the first.
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We found that the dramatic decreases in the rostral and caudal oscillations do not depend on the odorant that is presented, similar changes occur irrespective of whether the odorants in the two presentations are the same or different (e.g., Fig. 2, top and bottom). The rostral oscillation (top) to the second odorant presentation was substantially reduced or completely abolished at both odorant concentrations illustrated, 1.7 and 10%, independent of whether the second odorant was the same or different. Similarly, the low-frequency component of the caudal oscillation (bottom) was greatly reduced in response to the second presentation at both odorant concentrations and for all four presentation pairs.
However, for the middle oscillation the situation was very different—if the odorant at the second presentation was the same as at the first, the middle oscillation increased in size and/or duration. In contrast, if the odorant presented on the second stimulation was different, the middle oscillation was significantly reduced or undetectable (e.g., Fig. 2, middle). The change in middle oscillation did not depend on the identity of the odorant itself but on its relation (i.e., same or different) to the odorant presented in the first stimulus.
Similar changes to those illustrated in Figs. 1 and 2 were also observed for odorant concentrations of 0.3% of saturated vapor (data not shown), and thus these changes appear to be independent of odorant concentration over the range we tested.
The changes of the oscillatory response were relatively consistent across animals. To quantify the observed changes in the oscillatory response we measured the amplitude of the signals on sections of the recordings in 175 trials from 20 preparations. These preparations were selected for their large oscillatory response and included the experiments in Figs. 1 and 2. The labeled horizontal lines in Fig. 1, A and B, indicate the sections of that trial used to determine the power at the peak frequency of the oscillation from Fourier transforms. A measure of the change in power, C± SE, at the peak frequency of the observed oscillations, is plotted in Fig. 3. The measure, C, takes values between –1 and 1. An increased oscillation will yield positive values of C, whereas a decrease will result in negative values. The mean reduction of the power of rostral and caudal oscillations in the second presentation is large, and the reductions are independent of whether the odorants in the two trials are the same or different. In contrast, the direction of the change in the middle oscillation is strikingly dependent on whether the odorant presented in the two trials was the same or different. Similar histograms are obtained when the results for three different odorants used in the first presentation are plotted independently (Fig. 3, B–D).
The direction of the change (increase or decrease) for all of the trials in the preparations we studied is summarized in Table 1. In some preparations, the middle oscillation could not be detected in response to the first odorant presentation but was clearly seen in the second presentation of the same odorant (Fig. 5). An example of this kind of result is shown in Fig. 4 (see also Fig. 5). Instances of this sort were included in the groups indicated (*) in Table 1. The number of trials used for each percentage is indicated by the T values in parentheses.
One source for changes in the response to multiple presentations might be adaptation of the olfactory receptor neuron input to the bulb. We examined this hypothesis by imaging the increases of calcium concentration in the presynaptic terminals of the receptor neurons in the glomeruli (Wachowiak and Cohen 2001; Wachowiak et al. 2002) in response to repeated odorant presentations. The Calcium Green-1 signals from two locations in the dorsal bulb where we found the largest response to the two odorants, cineole and isoamyl acetate, are shown in Fig. 6. The calcium increase, as expected, was on average smaller in response to the second stimulation than to the first. This decline in response may in part be due to receptor adaptation from odorant that is not cleared from the olfactory epithelium between trials. However, the calcium increase after the second odorant presentation was somewhat larger when a different odorant was presented than when the same odorant was applied twice (Figs. 6 and 7). Thus because receptor adaptation is odorant dependent, it could only partially explain the decline of the rostral and caudal oscillations that are independent of odorant (Figs. 2 and 3). Furthermore, the observed changes in the amplitude of the middle oscillations are inversely correlated to the changes in the input to the bulb. Clearly, the changes in the oscillations in response to the second presentation must also reflect internal processing in the bulb or feedback from higher brain regions.
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DISCUSSION |
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Mechanisms responsible for the changes in response that occur on repeated presentations
Multiple mechanisms might account for the observed changes in the oscillatory response(s). The reduction of the rostral and caudal responses on the second odorant pulse could be partially due to the decreased input to the bulb. However the decreased input is smaller than the reduction of oscillations, and the decrease in input is somewhat dependent on whether the odorant is the same or different (Fig. 7), whereas the decrease in rostral and caudal oscillation amplitudes is independent of odorant (Fig. 3).
The olfactory bulb receives several kinds of feedback from higher centers (Pinching and Powell 1972; Scott and Harrison 1991). Extrinsic afferents primarily from the anterior olfactory nucleus synapse on periglomerular cells and, to lesser extent, on mitral/tufted cell dendrites (Luskin and Price 1983; Macrides and Davis 1983). Longer feedback loops involve the commissural projection system, which includes topographically organized mitral/tufted cell projection to the anterior olfactory nucleus the cells of which in turn project to a region of the contralateral bulb homotopic to the region of the ipsilateral bulb from which they received the input (Davis et al. 1978; Schoenfeld and Macrides 1984; Scott 1985). Corresponding regions of the two bulbs thus indirectly receive feedback from each other. Those projections terminate in the granule as well as glomerular layer (Luskin and Price 1983; Macrides and Davis 1983) and are predominantly excitatory thereby causing an inhibitory effect. This feedback mechanism can be powerful. In preliminary experiments, we found that conditioning of the olfactory bulb oscillations by prior stimulation of the contralateral (with respect to the imaged bulb) nares results in large changes in oscillations similar to those illustrated in this paper in response to repeated odorant presentations. (B. Singer, S. Kim, and M. Zochowski, in preparation).
A third major source of feedback is piriform cortex. Electrophysiological evidence suggests that pyriform cortex projections also make excitatory synapses onto granule cells and their stimulation inhibits mitral/tufted cells (Nakashima et al. 1978).
The reduction of the middle oscillation after the presentation of a different odorant as the second stimulus might be due to lateral presynaptic inhibition known to exist in the turtle (Wachowiak and Cohen 1999) and mammals (Shepherd and Greer 1998) or negative feedback from higher cortical regions as described in the preceding text. The increase in the middle oscillation after presentation of the same odorant as the second stimulation could be due to long-lasting self-excitation of the mitral/tufted cells (Salin et al. 2001; Schoppa and Urban 2003; Schoppa and Westbrook 2001) or could point to the existence of extrinsic excitatory cortical feedback.
Interruption of the lateral olfactory tract inhibits beta band oscillations in the bulb while leaving the gamma band oscillations unchanged (Neville and Haberly 2003). This result suggests an important role of feedback from pyriform cortex in modulation of the observed bulbar oscillations. In separate work, we have used computer simulations (S. Kim, B. Singer, M. Zochowski, unpublished data) to indicate that the period doubling transition from fast caudal (14 Hz) to slow caudal oscillation (7 Hz) could be mediated through lateral olfactory tract feedback from cortical regions.
Comparison with olfactory bulb oscillations in other animals
INCREASED OSCILLATIONS FOLLOWING REPEATED PRESENTATIONS.
We found that the middle oscillation in turtle increased in amplitude with repeated presentations if the same odorant was presented. Similar results were obtained in earlier measurements on locusts (Laurent and Naraghi 1994; Stopfer and Laurent 1999) and for some odorants in moths (Heinbockel et al. 1998). In agreement with Stopfer and Laurent (1999), we found that the over-all levels of input to the bulb (Fig. 6) declined on repeated odorant presentations while there was a significant increase of the oscillatory response in the middle oscillation. In contrast, a substantial difference between our findings and those in insects is that two of the oscillations (rostral and caudal) dramatically declined on repeated odorant presentations, independent of the odorants applied.
LOCALIZATION OF THE OSCILLATIONS.
All three oscillations in the turtle olfactory bulb cover substantial areas of the bulb, 1 mm2, which encompass hundreds of individual glomeruli (Lam et al. 2000, 2003). Similarly, the oscillations in the locust appear to be identical over the whole mushroom body (Laurent and Naraghi 1994). In dramatic contrast, oscillations in the moth are apparently localized to individual glomeruli (Christensen et al. 2003; Okada and Kanzaki 2001).
ODORANT DEPENDENCE.
All three oscillations in the turtle occur after relatively long (500–1,000 ms) latencies (Lam et al. 2000). These latencies are much longer than recent reports of the time required for olfactory discrimination in the rat (Abraham et al. 2004; Uchida and Mainen 2003). However, other measurements of sniff durations in discrimination experiments were closer to 1 s (e.g., Slotnick and Schellinck 2002; Youngentob et al. 1987). In addition, it is commonly observed that mammals will repeatedly sniff for several seconds at objects of interest. Thus the long latencies for the turtle oscillations probably cannot be used to rule out a role in odor discrimination.
In the locust, the oscillations can be different for different odorants and it is proposed that odorant quality is encoded in the spike activity of neuronal assemblies that is phase locked to the oscillations (Laurent and Davidowitz 1994; Stopfer et al. 1997). In contrast, the three oscillations in the turtle olfactory bulb can be very similar for odorants that have qualitatively different input maps to the bulb (Lam et al. 2003). Similarly, in the moth, zebrafish, rat, and rabbit, different odorants elicit similar oscillations (Adrian 1950; Christensen et al. 2003; Di Prisco and Freeman 1985; Friedrich et al. 2004; Lowry et al. 2005). Furthermore young rats can discriminate odorants quite well in the absence of measurable 
or 
oscillations (Fletcher et al. 2005). Thus Adrian's (1942) original conjecture that the oscillations in mammals were involved in odorant recognition appears to be incorrect.
STATE DEPENDENCE.
Ravel et al. (2003) and Martin et al. (2004) found that the sniffing of odorants decreased the band oscillation and increased the band oscillation in the rat olfactory bulb. In a related observation, Kay (2003) found that sniffing decreased the low-frequency (40–60 Hz) band power but increased the high-frequency (70–100 Hz) power. These findings are similar to our results in that they suggest that the oscillations in mammals subserve higher-order functions.
Thus it seems reasonable to conclude that the oscillations have different roles in different olfactory systems. Oscillations appear to be a neurophysiological mechanism that is adopted for different purposes by different animals. However, it remains possible that in any particular instance oscillations might be an epiphenomenon of network activity and have no cognitive function. Evidence concerning this possibility awaits a better understanding of olfactory processing.
In conclusion, our results suggest roles for the oscillatory response in turtles. One possible role of the oscillations is to provide an assessment of the novelty of the odorant. The increase in the middle oscillation that occurs in response in repeated presentation of the same odorant is blocked if the odorant is changed. This kind of response would be useful for recognition of odor quality consistency in while navigating in a complex, time-varying odorant plume. On the other hand, the dramatic (odorant independent) decreases in rostral and caudal oscillation may be part of the mechanism for odor accommodation or for alerting the nervous system to an important change in the odor environment. Consistent with this role is the finding that the rostral and caudal oscillation are elicited by relatively high odorant concentrations in the rabbit and turtle (Adrian 1950; Lam et al. 2000) as are oscillations in the rat (Lowry et al. 2005).
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. Zochowski, Dept. of Physics and Biophysics Research Div., University of Michigan, Randall Laboratories, 500 E. University Ave., Ann Arbor, MI 48109 (E-mail: michalz{at}umich.edu)
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INTRODUCTION
F, divided by the resting fluorescence, F. The largest voltage-sensitive dye signals were fractional changes of 
