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INTRODUCTION |
Convergence of inputs from bilateral receptive fields is a common feature of vertebrate sensory systems. This bilateral convergence allows for relative comparisons of spatially disparate inputs that can result in higher-order sensory processes such as depth perception in vision and stimulus localization in audition.
In the mammalian olfactory system, the stimulus enters two relatively isolated air passages through the external nares. Within each air passage is an olfactory receptor sheet, which in turn projects ipsilaterally to the main olfactory bulb (MOB). Mitral/tufted cells in the olfactory bulb project to the olfactory cortex, which is composed of several subregions including the anterior olfactory nucleus, the cortical nucleus of the amygdala, and the piriform cortex (Price 1987
).
It has been demonstrated anatomically that bilateral, or binaral, convergence occurs at most central olfactory structures (Haberly and Price 1978
; Luskin and Price 1983
). These interhemispheric connections are carried through the anterior limb of the anterior commissure. For example, in the olfactory bulb, input from the ipsilateral naris reaches the apical dendrite of mitral/tufted cells, whereas the most direct input from the contralateral naris terminates on inhibitory interneurons called granule cells (Price and Powell 1970
). In the piriform cortex, however, binaral convergence occurs within different subfields of the apical dendrites of layer II and III pyramidal neurons (Friedman and Price 1984
). Fibers from the ipsilateral olfactory bulb (ipsilateral naris) compose the lateral olfactory tract (LOT) and terminate in the piriform cortex superficial layer Ia, whereas commissural fibers from the contralateral hemisphere (contralateral naris) terminate in the deeper layer Ib, along with intracortical association fibers (Haberly 1985
; Haberly and Price 1978
; Luskin and Price 1983
). In the anterior piriform cortex (aPCX), the source of these commissural fibers is primarily the contralateral pars lateralis of the anterior olfactory nucleus, which receives direct input from the olfactory bulb (Luskin and Price 1983
). Fibers in layers Ia and Ib form excitatory synaptic connections with pyramidal neurons (Haberly 1985
; Haberly and Bower 1984
).
These anatomic data suggest that single piriform cortex pyramidal neurons may have binaral response properties
that is, they may perform relative comparisons between activity in the two olfactory receptor sheets
similar to the binocular cells of the primary visual cortex. To date, there have been relatively few single-unit examinations of mammalian piriform cortex odor response patterns and all have relied on bilaterally presented odors (Duchamp-Viret et al. 1996
; Giachetti and MacLeod 1975
; Haberly 1969
; McCollum et al. 1991
; Nemitz and Goldberg 1983
; Schoenbaum and Eichenbaum 1995
; Tanabe et al. 1975
). These studies have found that piriform cortex units respond to odors with relatively short latencies and with a variety of temporalpatterns.
The present report examines aPCX single-unit responses to ipsilateral and contralateral olfactory bulb inputs. Two approaches were used. First, odors were delivered unilaterally through tubes inserted into the nares while olfactory bulb activity was simultaneously monitored bilaterally to confirm localization of the stimulus. The second method involved unilateral olfactory bulb lidocaine application to reversibly block ipsilateral or contralateral olfactory bulb activity during bilateral odor presentations. The results demonstrate that commissural input can drive aPCX unit responses to odors, and that, in addition to odor/molecular receptive fields, aPCX single units have spatially defined (ipsilateral/contralateral) receptive fields.
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METHODS |
Subjects
Eleven male Wistar rats (150-350 g) obtained from Charles River Labs were used as subjects. Animals were housed in polypropylene cages lined with wood chips. Food and water were available ad libitum. Lights were maintained on a 12:12 light:dark cycle with testing occurring during the light portion of the cycle.
Electrophysiology
Animals were anesthetized with urethan (1.5 g/kg) and placed in a stereotaxic apparatus. Both olfactory bulbs were exposed through holes drilled in the dorsal surface of the skull and a third hole drilled over the aPCX, ~1 mm anterior to bregma. Recordings were made with tungsten microelectrodes (5-12 M
, A-M Systems).
Olfactory bulb activity was monitored with the use of simultaneous, bilateral multiunit or slow-wave recordings. Multiunit activity was recorded in the olfactory bulbs by lowering a tungsten microelectrode into the ventral mitral cell body layer, approximately in the middle of the anterior-posterior extent of the bulb. Multiunit activity was band-pass filtered (300 Hz-3 kHz) and passed through a window discriminator. Multiunit odor responses were monitored with peristimulus time histograms. In some animals, slow-wave activity was recorded in the ventral mitral cell body layer with tungsten microelectrodes, band-pass filtered (0.3 Hz-1 kHz), and sampled at 1 kHz. Slow-wave activity was quantified with fast Fourier transform (FFT) power spectrum analysis of 4-s time periods during odor stimulation with the Spike2 software package.
Single-unit activity was recorded in the aPCX. The tungsten recording electrode (5-12 M
) was lowered from the dorsal skull surface. Placement of the recording electrode in layer II/III of the piriform was performed under physiological control by electrically stimulating (pulse duration 0.1 ms; 50-500 µA) through the ipsilateral olfactory bulb recording electrode. Recordings were performed at, or slightly dorsal to, the reversal point of the population potential evoked by ipsilateral bulb stimulation (Haberly and Shepherd 1973
). Single units were isolated directly, or were extracted through template matching (sampling rate 10 kHz) with the use of Spike2 software for the Macintosh (CED). The single-unit nature of the recordings was confirmed with autocorrelograms showing a refractory period of
3 ms.
After the recording session, the location of the electrode tip was marked by electrolytic lesions, and placements in the aPCX were confirmed histologically.
Unilateral odor stimulation
For unilateral odor stimulation, an odor delivery device was inserted into both nares (Fig. 1). Animals were freely breathing through both nares at all times. The device consisted of a short piece of PE160 tubing connected to the narrow end of a modified Eppendorf pipetter tip (5 cm long, 0.5 cm ID at wide end). The PE160 tubing was placed into the external naris. An odor port was inserted through the wall of the pipette tip with the use of PE60 tubing. The devices were angled to create a distance of
3-4 cm between clean air intake sites (wide end of the pipette tip). A humidified, clean air stream (1 l/min) was directed downward over the two devices to minimize odorant diffusion out of one device to the contralateral device. Stimuli were produced with a Hamilton model 22 syringe pump controlled with a Macintosh computer and Spike2 software. The syringe pump forced air across odorant (isoamyl acetate, Sigma)-saturated filter paper to present the odor through the odor ports. Odors were presented unilaterally or bilaterally through computer-controlled solenoids that directed the odor stream (10-25 ml/min) to one or the other device. Within an animal, all stimuli were delivered at the same volume per minute, i.e., the total volume of odor delivered during bilateral stimulation matched the total volume delivered during unilateral stimulation. Stimulus duration was 4 s, and both olfactory bulb and aPCX activity during the odor were compared with a 4-s preodor baseline. Interstimulus intervals were
60 s. Each stimulus (ipsilateral, contralateral, or both) was repeated at least three times and order of presentation was varied within and between cells.

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| FIG. 1.
Uninaral stimulation apparatus. Air was forced through odorant-saturated filter paper by computer-controlled activation of a syringe pump and simultaneous opening of a solenoid valve. Odor was delivered to a device inserted into the animal's naris, and inhaled by normal respiration, as described in METHODS. Humidified clean air was directed over the open end of the delivery devices.
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Unilateral lidocaine application
To further examine the unilateral nature of odor response patterns, a second paradigm in which the more common method of bilateral odor stimulation with odorant delivery to the external nares was used was combined with unilateral lidocaine blockade of olfactory bulb activity. Odors were presented bilaterally through a tube ~1 cm in front of the external nares. Animals were freely breathing. A clean, humidified air stream (1 l/min) was blown constantly across the snout of the animal to exhaust odors. Stimuli were created as above, by forcing air through odorant-saturated filter paper with a syringe pump. After collection of bilateral control data, lidocaine (5-10 µl, 2% solution; Astra Pharmaceutical Products) was applied to the surface of either the ipsilateral or contralateral olfactory bulb (relative to the aPCX recording). The duration and unilateral specificity of the lidocaine effect was monitored with the olfactory bulb recordings, and odor stimulation was repeated both during the maximal lidocaine suppression and, if the stability of the aPCX recording allowed, after recovery. Spontaneous aPCX single-unit activity rates were also monitored for
100 s before and 5 min after lidocaine application.
Response analysis
aPCX single-unit odor responses were analyzed with the use of cumulative peristimulus time histograms with either 0.1- or 0.2-s binwidths, including activity during a 4-s preodor baseline and the 4 s of odor for at least three stimulus repetitions. A single unit was determined to have responded to the stimulus if cumulative firing rate in any bin during the stimulus was above baseline variability. This measure, which has been used in the olfactory bulb (Wilson et al. 1985
), was chosen because, as previously reported (McCollum et al. 1991
) and as described below, aPCX single-unit odor responses were frequently very brief and habituated rapidly. Furthermore, preodor spontaneous activity was often very slow or silent (especially in the lidocaine experiments), thus precluding statistical comparison of preodor versus postodor firing rates. Because our objective was to describe the frequency of occurrence of ipsilaterally and contralaterally driven responses, the most important requirement was to apply a constant, sensitive criterion in all circumstances. This measure satisfies that requirement. Because of variability of responses, no attempt was made to quantify response magnitude for comparisons of relative effectiveness of ipsilateral versus contralateral inputs.

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| FIG. 2.
Anterior piriform cortex (aPCX) single-unit response to isoamyl acetate delivered bilaterally and unilaterally through tubes inserted into the nares. A: bilateral odor presentation produced a robust aPCX excitatory response. B: unilateral odor presentation to ipsilateral naris selectively activated ipsilateral main olfactory bulb (MOB) as shown in histograms of multiunit activity recorded simultaneously in ipsilateral and contralateral MOB. aPCX single unit responded to this ipsilateral stimulation. C: unilateral odor presentation to contralateral naris selectively activated contralateral MOB. aPCX unit also responded to this contralaterally delivered odor stimulus. D: single-unit nature of this and all recordings was verified with autocorrelation analysis.
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RESULTS |
A total of 70 single units was recorded from aPCX layers II/III in 10 animals. Of these, 32 cells were tested for responses to unilaterally delivered odors, and 38 cells were tested for spontaneous activity and/or odor responses during unilateral olfactory bulb lidocaine application. Simultaneously, olfactory bulb activity was recorded bilaterally in all animals to monitor and confirm the unilateral nature of odor stimulation and lidocaine actions. Olfactory bulb multiunit responses to odor were characterized by robust excitation. Olfactory bulb slow-wave responses to odors were characterized by large-amplitude waves in phase with respiration, as previously reported (Adrian 1950
). Both of these measures were reliable and sensitive indicators of odor stimulation. aPCX single units responded to odor stimulation most frequently with excitation, and very rarely with suppression in our sample. This excitation generally did not last through the entire 4-s odor stimulus (e.g., Figs. 3 and 7).

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| FIG. 3.
Unilateral odor presentation could result in "cross talk" between nasal passages. Stimulus rates were adjusted within animals to eliminate cross talk. This figure shows simultaneous bilateral multiunit recording of MOB activity and single-unit recording of aPCX activity in response to odor presented to the naris ipsilateral to the aPCX recording (stimulus presentation marked by horizontal bar). Top: when the odor was presented at a high rate (25 ml/min), leakage occurred between nasal passages, possibly through the septal window, such that both MOBs responded. Bottom: at lower stimulus rates (10 ml/min) no leakage occurred between hemispheres. Note aPCX unit responded to odor in both conditions.
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| FIG. 7.
aPCX single-unit and simultaneous MOB slow-wave response to bilateral odor presentation before and after lidocaine application on ipsilateral MOB. Ipsilateral lidocaine dramatically reduced aPCX spontaneous activity, but did not block the aPCX odor response despite dramatically reducing ipsilateral MOB slow-wave activity. Fast Fourier transform (FFT) analysis showed that contralateral MOB slow-wave activity was not reduced by lidocaine infusion.
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Unilateral odor presentation
Figure 2 is a representative example of an aPCX single-unit response to odor stimulation of either the ipsilateral or contralateral naris. The same aPCX unit is shown for each stimulus. Bilateral odor stimulation (Fig. 2A), produced a rapid increase in this cell's activity. Similar excitatory responses were observed to unilateral odor stimulation delivered to either naris. For example, odor presented to the ipsilateral naris (Fig. 2B) selectively activated the ipsilateral olfactory bulb and excited the aPCX unit. Odor presented to the contralateral naris (Fig. 2C) selectively activated the contralateral olfactory bulb and also excited the aPCX unit. Figure 2 thus is an example of a binaral aPCX unit with bilateral receptive fields.
Unilateral odor presentation could, however, result in "cross talk" between nasal passages, where a stimulus presented to one naris excited both olfactory bulbs. In these cases, stimulus rates were adjusted within each animal to eliminate cross talk. Figure 2 shows simultaneous bilateral multiunit recordings of MOB activity and single-unit recording of aPCX activity in response to odor presented to the naris ipsilateral to the aPCX recording. When the odor was presented at a high rate/concentration (25 ml/min; Fig. 3, top), leakage occurred between nasal passages, possibly through the septal window, such that both olfactory bulbs responded. At lower stimulus rates/concentrations (10 ml/min; Fig. 3, bottom) no detectable leakage occurred between hemispheres. Note that the aPCX unit responded to the odor in both conditions. The remainder of the data presented here used stimuli that did not result in detectable cross talk.
A total of 32 aPCX single units in five animals was tested with the use of the single-naris stimulation paradigm. The aPCX response types were subdivided into specific response patterns, including cells that 1) responded selectively to ipsilateral naris stimulation, 2) responded selectively to contralateral naris stimulation, 3) responded to either ipsilateral or contralateral stimulation, or 4) responded selectively to bilateral stimulation (ipsi- and contralateral simultaneously) but not to unilateral stimulation. (Most cells in categories 1-3 also responded to bilateral stimulation; cells in category 4 only responded to bilateral stimulation.)
aPCX units matching some or all of these response patterns were observed within each animal. For example, in three of the five animals tested, both cells responding selectively to the ipsilateral naris and cells responding selectively to the contralateral naris were observed. In one animal, cells representative of all four response groups were observed. In addition, MOB odor response magnitude did not dramatically vary over the course of single recording sessions, suggesting that nasal patency did not vary markedly within sessions. Finally, in at least one animal, a unit responding selectively to the ipsilateral naris was recorded simultaneously (with template matching) with a unit responding selectively to the contralateral naris. These observations suggest that unilateral response patterns are not due to lateralized differences in nasal resistance or stimulus concentration differences in single animals, but rather reflect real differences in receptive fields of aPCX neurons for isoamyl acetate.
Total response rates (% of cells responding to a given stimulus location) were determined for each stimulus condition in each animal, and response rates (means ± SE) across animals are presented in Fig. 4. For this sample of neurons, in this location of the aPCX, and with this odor, each of the spatial receptive fields was nearly equally represented. Nearly 10% of the recorded cells only responded if the stimulation was presented bilaterally (as described in METHODS, total stimulus volume was the same for unilateral and bilateral stimuli). As discussed below, different patterns of receptive field frequencies may be observed in other regions of the PCX or with other odors.

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| FIG. 4.
aPCX single-unit odor response patterns to bilateral and unilateral stimulation through naris tubes. Selective response patterns including cells that responded to ipsilateral stimulation but not contralateral stimulation, that responded to contralateral stimulation but not ipsilateral stimulation, that responded to either ipsilateral or contralateral stimulation, and that responded only to bilateral stimulation. Values are means ± SE.
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When specific categories are ignored, 35 ± 9% (mean ± SE) of cells in our sample responded to bilateral stimulation, a rate comparable with other reports of rat piriform odor responsiveness (McCollum et al. 1991
; Nemitz and Goldberg 1983
).
Unilateral olfactory bulb lidocaine application
A total of 38 aPCX single units in five animals was tested for the effects of unilateral olfactory lidocaine application on spontaneous activity (ipsilateral lidocaine, n = 21; contralateral lidocaine, n = 21; 3 cells were tested in both conditions). Lidocaine application on the dorsal surface of the olfactory bulb significantly reduced olfactory bulb activity as determined by complete cessation of multiunit activity (e.g., Fig. 6) or drastic reduction in odor-evoked slow-wave activity recorded in the ventral mitral cell layer (e.g., Fig. 7). Maintenance of some slow-wave activity during lidocaine application might be expected because of the contribution of remaining subthreshold synaptic activity to this measure. The bilateral bulb recordings demonstrated that lidocaine application produced selective unilateral effects on bulb activity (e.g., Figs. 7 and 8).

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| FIG. 6.
aPCX single-unit and ipsilateral MOB multiunit response to bilateral odor presentation before (top) and after (bottom) lidocaine application on ipsilateral MOB. Lidocaine resulted in total blockade of ipsilateral MOB multiunit activity (bottom left), yet the aPCX single unit continued to respond to odor stimulus (bottom right).
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| FIG. 8.
aPCX single-unit and simultaneous MOB slow-wave response to bilateral odor presentation before and after lidocaine application on ipsilateral MOB. In this example, the aPCX single-unit spontaneous activity and odor response were blocked by ipsilateral MOB lidocaine infusion. Responses returned as lidocaine effect diminished.
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Lidocaine application on the olfactory bulb ipsilateral to the aPCX recording resulted in a 92% decrease in spontaneous aPCX unit activity (sampled during a 100-s period at the peak of the lidocaine effect; Fig. 5, A top). Importantly, lidocaine applied to the contralateral olfactory bulb (Fig. 5, A middle) also resulted in a significant decrease in spontaneous aPCX unit activity of nearly 50% (1-sample t-test vs. hypothesized mean change of 0%; ipsilateral lidocaine t(20) =
92.9, P < 0.001; contralateral lidocaine, t(20) =
54.5, P < 0.001; Fig. 5B).

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| FIG. 5.
aPCX single-unit spontaneous activity following unilateral lidocaine surface application onto either ipsilateral or contralateral MOB. Ipsilateral application resulted in a nearly complete cessation of aPCX activity, whereas contralateral applications resulted in a 50% decrease in spontaneous activity.
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Despite the lidocaine-induced elimination of multiunit activity, and/or dramatic reductions in slow-wave activity in the ipsilateral olfactory bulb, some aPCX units maintained odor responsiveness to bilaterally presented odors, suggesting a contralateral source of activation (Figs. 6 and 7). These responses were generally expressed against a greatly reduced background firing rate. For example, Fig. 6 shows multiunit olfactory bulb activity recorded ipsilaterally to aPCX single-unit activity before (top) and after (bottom) olfactory bulb lidocaine application. Despite complete elimination of ipsilateral olfactory bulb multiunit activity by the lidocaine, the aPCX unit continued to respond to the bilaterally presented odor (Fig. 6, bottom right). Recall that olfactory bulb recordings were made from the ventral mitral cell body layer and lidocaine applications were made on the dorsal bulb surface. Thus these recordings are most probably indicative of suppression throughout the bulb.
Another example of maintained aPCX unit odor responses during ipsilateral olfactory bulb lidocaine is shown in Fig. 7. In this example, bilateral olfactory bulb slow-wave recordings showed typical, large-amplitude slow-wave oscillations during bilateral odor stimulation, and the simultaneous aPCX single-unit recording showed an excitatory response to the odor (Fig. 7, top). After lidocaine application to the ipsilateral olfactory bulb (Fig. 7, middle), the ipsilateral bulb slow-wave response was dramatically reduced, yet the aPCX unit response, although diminished, remained. FFT analysis of olfactory bulb activity before and after lidocaine application (Fig. 7, bottom) demonstrated that the lidocaine selectively depressed the olfactory bulb ipsilateral to the aPCX recording.
In other aPCX units, ipsilateral olfactory bulb lidocaine blocked odor responsiveness, suggesting that these units were either not responsive to contralateral activation or were so depressed that contralateral inputs were insufficient to produce detectable responses. For example, as shown in Fig. 8, top, bilateral odor exposure produced bilateral olfactory bulb slow-wave responses and an excitatory response in the simultaneously recorded aPCX unit. Lidocaine application on the olfactory bulb ipsilateral to the aPCX recording (Fig. 8, middle) eliminated both the ipsilateral bulb response and the aPCX unit response to odor. After recovery from the lidocaine suppression of bulb activity (Fig. 8, bottom), the aPCX unit odor response recovered. Furthermore, bilateral lidocaine application eliminated all odor responses, suggesting that the aPCX unit responses reflect odor responsiveness and are not trigeminally mediated.
As shown in Fig. 9, a mean of 52% of the aPCX cells in this sample (21 cells, 5 animals) responded to bilaterally presented odor. After ipsilateral olfactory bulb lidocaine application, 21% of the cells continued to respond to the odor, presumably via direct commissural activation.

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| FIG. 9.
Percent of aPCX single units responding to bilateral odor stimuli before and after lidocaine application to ipsilateral OB. Despite elimination of detectable ipsilateral olfactory bulb activity, 21% of cells maintained odor responses.
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As a final test of the contralateral nature of odor driven responses, in a single animal the olfactory bulb ipsilateral to the aPCX recording site was aspirated. Within 2 h postaspiration, multiunit aPCX responses to bilaterally presented odors were observed (not shown). Subsequent histological analyses showed complete tissue removal and damage extending caudal to the accessory olfactory bulb. Furthermore, the ipsilateral olfactory epithelium was damaged, as evidenced by minor bleeding from the ipsilateral naris. The odor responses, in the absence of an ipsilateral olfactory bulb, are further evidence of contralaterally driven odor input to the aPCX.
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DISCUSSION |
The present results demonstrate that aPCX layer II/III single units can respond to unilateral odor stimulation of the contralateral naris. Furthermore, these results suggest that, similar to monocular and binocular receptive fields of mammalian visual cortical neurons, aPCX neurons have mononaral and binaral receptive fields.
aPCX responsiveness to contralateral naris stimulation could be mediated by 1) odor leakage through the septal window, 2) interbulbar interactions such that the contralateral bulb somehow activated the ipsilateral bulb to in turn excite the aPCX, or 3) direct commissural input to the aPCX from the contralateral hemisphere. First, although odor leakage can occur (Fig. 3), the bilateral olfactory bulb recordings showed selective unilateral bulb activation to unilaterally presented odors, and thus no detectable cross talk between passages. Furthermore, aPCX units continued to respond to odors despite verified lidocaine suppression of the ipsilateral bulb.
The second potential mechanism, interbulbar interaction, does occur but cannot account for the present results. Interolfactory bulb interaction is primarily inhibitory to mitral/tufted cells in the rat (Price and Powell 1970
; von Baumgarten et al. 1962
). In the present study, evidence of this interbulbar inhibition was seen in the lidocaine experiments. In several cases, unilateral olfactory bulb blockade with lidocaine enhanced the magnitude of contralateral bulb odor responses, as seen quantitatively in the FFT analysis in Fig. 7 and qualitatively in the slow-wave amplitude of olfactory bulbs contralateral to lidocaine-suppressed bulbs (Figs. 7 and 8). Thus, if the interbulbar interaction influenced aPCX activity, it might be expected to reduce the probability of observing aPCX unit odor responses. Instead, we observed contralaterally driven excitation of aPCX units. Furthermore, as shown above, aPCX units continued to respond to odors despite lidocaine suppression of the ipsilateral bulb.
These results suggest, therefore, that aPCX responses to contralateral naris stimulation are mediated by direct commissural input to the aPCX, rather than indirectly through internasal cross talk or interbulbar connections. Further evidence for a direct, functionally significant commissural input to the aPCX comes from the olfactory bulb lidocaine effects on spontaneous aPCX activity. Blockade of contralateral olfactory bulb activity produced a 50% decrease in aPCX spontaneous activity (Fig. 5). Although the magnitude of this effect was significantly less than that observed for ipsilateral bulb suppression, it suggests a relatively strong, tonic excitatory input to the aPCX mediated by commissural fibers. The primary route for these fibers involves the MOB projection to the anterior olfactory nucleus pars lateralis, which in turn projects via the anterior commissure to aPCX layer Ib (Luskin and Price 1983
).
Potential anatomic substrates of spatial receptive fields
The relatively similar proportion of ipsilaterally and contralaterally driven mononaral aPCX neurons was surprising given the relatively low density of commissural fibers compared with LOT fiber density in the rat aPCX (Friedman and Price 1986
). However, as stated above, commissural fibers terminate in the proximal half of the apical dendritic tree, and thus are electrotonically closer to the axon hillock than LOT fiber terminals. In addition, LOT fibers, but not commissural fibers, are believed to activate feedforward inhibitory interneurons, which could produce a relative weakening of ipsilateral input (Kanter et al. 1996
).
Furthermore, the aPCX contains a variety of principle neuron morphologies, which could account for the different spatial receptive fields reported here. For example, semilunar pyramidal-type cells with somata located in superficial layer II have reduced basal dendrites and extend multiple apical dendrites through both layers Ib and Ia. However, these dendrites have very few spines within layer Ib and dense, large spines within layer Ia (Haberly 1983
; Heimer and Kalil 1978
). Thus semilunar cells might be expected to receive strong input from the ipsilateral LOT and limited input from associational/commissural fibers. In fact, bulbectomy results in a selective, rapid die-off of semilunar cells in the ipsilateral aPCX (Heimer and Kalil 1978
). As another example, although most layer II/III pyramidal neurons have apical dendrites extending through both layers Ib and Ia, a subclass of layer III pyramidal cells has apical dendrites that end in profuse branching at the layer Ib/Ia border (Haberly 1983
). Thus these cells might be expected to receive primarily association/commissural input and very limited ipsilateral LOT input.
Another potential anatomic substrate of, or factor contributing to, spatial receptive fields is the variation in density and thickness of layer Ia over the rostral/caudal and dorsal/ventral extent of the piriform cortex. Layer Ia is thickest near the LOT, and progessively thins in more lateral and caudal areas of the cortex (Schwob and Price 1984
). Thus the relative proportion of the four described spatial receptive fields as shown in Fig. 4 might be expected to vary with location within the piriform cortex.
Functional role of spatial receptive fields
The functional role of commissural connections and binaral receptive fields in olfactory coding is unknown. Although commissural connections are important in other sensory systems for stimulus localization, in humans simultaneous binaral comparisons do not appear sufficient to allow odorant source localization (in the absence of concomitant trigeminal activation) (Kobal et al. 1989
). However, lesion studies of olfactory guided behavior have suggested that the anterior commissure may be involved in at least two specific aspects of olfaction. First, lesions of the anterior commissure increase odor detection thresholds in rats (Bennett 1968
). These results were interpreted as suggesting that intact commissural connections increase perceived odor intensity, perhaps through an additive effect of bilateral stimulation on higher structures. The present finding that 10% of aPCX neurons required bilateral stimulation to produce a detectable response (Fig. 4) supports this hypothesis. Second, the anterior commissure appears to be critically involved in transfer of, or access to, olfactory memories acquired unilaterally in rats (Kucharski and Hall 1987
; cf. Olsson and Cain 1996
for humans). The observation here that aPCX neurons have binaral receptive fields may help account for this apparent information transfer. Unilateral olfactory training may modify both ipsilateral and contralateral aPCXs.
The finding of binaral receptive fields in aPCX should have important implications for our understanding of information coding in the olfactory system, as well as serve as an important paradigm for future work. For example, current research in our laboratory using this paradigm is addressing the following questions. 1) What is the role of experience in shaping binaral receptive fields (Wilson and Sullivan 1996
)? 2) Do binaral aPCX units have similar odor receptive fields on both sides (i.e., do they respond to the same set of odors ipsilaterally and contralaterally)? 3) Does habituation of aPCX unit responses to ipsilateral odors produce habituation to contralateral odors and vice versa?