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we present mechanistic and spatial dissections of olfactory discrimination, learning, and memory. We employed gene-targeted and transgenic mice with region-specific expression to demonstrate that a change in GluR-B-mediated properties of AMPA channels in αCaMKII-expressing neurons of mouse forebrain, including olfactory bulb mitral and granule cells, enhances olfactory discrimination and learning but impairs olfactory memory. These pertinent olfactory behaviors were assessed in a go/no-go operant conditioning task, which provides a quantitative, robust, and reproducible behavioral tool [3]. We observed among individual mice a striking variability in olfactory memory performance but not in odor discrimination. This variability could be traced to epigenetic variability in the transgenic expression of Cre-recombinase, which mediated recombination within loxP-flanked segments of gene-targeted alleles for the dominant AMPAR subunit GluR-B, and hence operated the switch in AMPAR properties toward GluR-B ablation and increased Ca2+ permeability. In contrast to variable memory, olfactory discrimination and learning performances appeared already saturated by even moderate extents of Cre expression, and hence moderate changes in AMPAR properties. The subsequent transgene-driven re-introduction of GluR-B, specifically in piriform cortex and hippocampus, reversed the Cre-induced loss of GluR-B and partially rescued the odor memory deficit, but left unaltered the enhanced olfactory discrimination. In a nutshell, we conclude that olfactory discrimination is enhanced by an increase in AMPAR-mediated Ca2+ permeability within the olfactory bulb, whereas olfactory memory becomes impaired upon genetically induced GluR-B ablation in higher brain centers, specifically in piriform cortex.\n\nOlfactory Discrimination Is Increased in Mice with Forebrain-Specific GluR-B Ablation or GluR-B(Q) Expression\nBoth forebrain-specific GluR-B(Q) expression and GluR-B depletion led to increased olfactory learning and discrimination capabilities. This was rather pronounced for GluR-B(Q)-expressing mice, consistent with the overall stronger phenotypic consequences in comparison to GluR-B depletion, both when forebrain-selective ([58], and this study) or global [53,60].\nA detailed analysis of the sampling pattern [3], and in particular the analysis of discrimination tasks that involved “simple” dissimilar monomolecular odor pairs and “difficult” binary mixtures, were necessary to fully capture the characteristics of the olfactory discrimination phenotype for forebrain-specific GluR-B-depleted mice. For closely related binary mixtures, discrimination improvements were largest, consistent with a specific alteration in odor discrimination, rather than a general enhancement of learning capabilities. This is further supported by the notion that no general improvement was observed in other nonolfactory behavioral tasks, e.g., hippocampus-dependent spatial learning tasks such as matching-to-place spatial reference memory tasks (Figure S2). As no Cre expression and activity was observed in the main olfactory sensory neurons at any developmental stage (Figure S4 and unpublished data), olfactory epithelial function was unaltered by the genetic modification. The vomeronasal organ showed very weak Cre expression (unpublished data), but a role of this structure concerning performance in the olfactory discrimination task is unlikely (for review, see [63]). The behavioral phenotype is thus likely to be associated with the processing of olfactory information rather than the detection of odors. Furthermore, increased performance even after long stretches of training and, in particular, increased sampling pattern differences (TB and ATS, unpublished data) supported the notion that GluR-B depletion resulted in enhanced odor discrimination capability. The learning phenotype might thus be a result of this enhanced discrimination capability or reflect additional changes in circuits underlying task acquisition.\n\nPutative Cellular Basis of Enhanced Odor Discrimination and Learning\nAMPAR properties were altered specifically in neurons of forebrain areas, most notably olfactory bulb, olfactory cortex, and other cortical areas and hippocampus, leading to enhanced odor discrimination and learning. Interestingly, transgenic expression of GFPGluR-B in GluR-BΔFB mice (genetic “rescue”), specifically in piriform cortex and hippocampus with no detectable expression in the olfactory bulb, did not alter enhanced discrimination and learning capabilities. This is consistent with a primary role of the olfactory bulb in olfactory discrimination and learning. Alternatively, transgenic protein levels might have been too low to alter discrimination and learning capabilities, although memory was clearly affected. This notion will be further tested in mice with piriform cortex-specific GluR-B ablation.\nA direct contribution to the phenotype by Ca2+ influx through genetically modified AMPA channels seems to be likely, since mice expressing Q/R site-unedited GluR-B showed even better odor learning and discrimination performance compared with mice with depleted GluR-B. In both mouse models Ca2+ influx through AMPA channels is increased, whereas the effect on the macroscopic AMPA conductance differs. AMPAR currents are reduced in mice not expressing GluR-B [51], possibly due to fewer synaptic AMPA channels and impaired AMPAR trafficking and recycling. In mice expressing the unedited form of GluR-B(Q), macroscopic conductance in whole-cell patches of CA1 pyramidals is increased [60], but excitatory transmission in CA3-to-CA1 cell synapses is somewhat reduced, in spite of a lower threshold for generating a population spike [58], indicating increased synaptic excitability by sustained GluR-B(Q) expression, in line with the seizure-prone phenotype. Yet, both mouse models yield enhanced discrimination and learning capability. The milder phenotype upon GluR-B depletion could be attributed to reduced AMPAR densities at synapses [40,41] and therefore probably to a lesser extent of Ca2+ influx. This is further supported by kainate-induced Co2+ uptake in acute brain slices, revealing considerably higher Co2+ uptake via Ca2+-permeable AMPARs in hippocampal pyramidal neurons of mice expressing GluR-B(Q), than those lacking GluR-B (DRS, RS, and PHS, unpublished data).\nNormally, GluR-B-containing AMPARs are prominently localized at the dendrodendritic synapse between mitral and granule cells in the olfactory bulb [64,65]. As Ca2+ influx through glutamate receptors is thought to contribute to lateral and recurrent inhibition ([38] see also [39]), the absence of GluR-B, or the presence of GluR-B(Q) in the olfactory bulb, is likely to result in increased inhibition between the principal neurons in this structure. Notably, the improved olfactory discrimination capabilities were apparent even upon relatively small reductions in GluR-B levels. It will be interesting to see if GluR-B+/neo mice also exhibit enhanced odor discrimination, which is indeed likely given that low levels of GluR-B(Q), and hence a small increase in Ca2+-permeable AMPARs, arise from the attenuated GluR-Bneo allele [60], and, moreover, that GluR-B levels are decreased in these mice due to the single copy of the GluR-B+ allele.\nIn virtually all models of the olfactory bulb, lateral (and, in fewer models, also recurrent) inhibition plays a dominant role, either in establishing spatiotemporal dynamics [32,66–69], or in directly enhancing contrast and therefore simplifying discrimination and learning of similar odorants [24,28,29,36]. Increased inhibition will thus in general improve discriminability, consistent with the behavioral improvements observed with GluR-B(Q) expression, the GluR-B knockout, and the “rescue” mice. A direct test of this link would require the quantitative measurement of inhibition in the intact preparation, a task that might be feasible with further improved in vivo electrophysiological techniques, such as targeted recordings [70,71] or simultaneous pre- and postsynaptic intracellular measurements.\n\nOlfactory Memory Is Reduced in GluR-B Knockout Mice and Improved by GluR-B Expression in Piriform Cortex and Hippocampus\nTo assess olfactory memory of GluR-BΔFB mice, after six days the mice were probed with unrewarded odor presentations that interleaved a simple discrimination task. Prolonged behavioral tasks such as the assessment of long-term olfactory memory were not performed with the seizure-prone GluR-BΔECS:FB mice. Memory in GluR-BΔFB mice, however, was dramatically impaired. This cannot be attributed to a general, unspecific deficit because, simultaneous to the memory trials, the normal, rewarded discrimination task was performed even better than by controls. Reduced olfactory memory can also not be simply attributed to increased extinction, as no significant trial-group interactions were observed and also, when restricted to the first unrewarded memory trials, a significant impairment was observed (Figure S3A). Additionally, investigating relearning of the first discrimination task revealed a significant correlation with the memory performance, showing a “memory” deficit under extinction-free conditions (Figure S3B). Finally, in other memory-related tasks, such as a hippocampus-dependent spatial reference memory task (Figure S2), mice with GluR-B depletion were not impaired after task acquisition. We therefore conclude that forebrain-specific ablation of GluR-B results in a specific loss of long-term olfactory memory but, at the same time, in enhanced odor discrimination and learning capabilities.\nTo dissect the discrimination, learning, and memory phenotypes, and ultimately identify potential cellular correlates, we made use of the variegated Cre expression of TgCre4 mice. Therefore, residual GluR-B levels were determined from each mouse that had been tested in the behavioral experiments, and levels were correlated with odor learning, discrimination, and olfactory memory. The significant direct correlation between residual GluR-B levels in hippocampus and cortical areas with olfactory memory suggested hippocampal and/or cortical neurons as putative mediators for odor memorization and/or storage. No measure of discrimination and learning, on the other hand, correlated with residual GluR-B levels; even the smallest reduction in GluR-B levels (about 20%–60%) was sufficient to establish and saturate enhanced odor discrimination capabilities. Together, this allows the conclusion that distinct mechanisms mediate discrimination/learning and memory. This is furthermore consistent with a prominent role of cortical areas or hippocampus in olfactory memory, although GluR-B levels in the olfactory bulb were also weakly correlated with memory performance. Transgenic expression of GFPGluR-B in piriform cortex and hippocampus indeed rescued memory to an extent strikingly consistent with the transgenic protein levels (approximately 10% of wild-type GluR-B), confirming the reliability of the correlation analysis and the sensitivity of the behavioral assay.\nIn general, the hippocampus is thought to be involved in only those olfactory memory tasks that involve temporal sequence analysis or require other higher cognitive features [2,13,72–74]. In particular, extensive lesions to the hippocampal formation in rats do not interfere with long-term olfactory memory in go/no-go successive olfactory discrimination tasks [72], such as the one described. This leaves piriform cortex as the most prominent candidate for the locus of the olfactory memory deficit described, consistent with the prevalent view of piriform cortex as an associational memory structure [75] and learning-associated changes in piriform cortex [7,20–23].\n\nPotential Mechanisms of Specific Olfactory Memory Impairment\nWhat could be the cellular basis of the long-term memory deficit brought about by lack of GluR-B-containing AMPARs? For complete GluR-B knockouts, increased long-term plasticity (LTP) was reported in hippocampal field recordings [51]. In addition, in hippocampal and amygdala pathways lacking GluR-B, an AMPAR-dependent, N-methyl-D-aspartate (NMDA) receptor-independent form of LTP can be readily induced [51,52]. Mechanistically, this is likely to be due to Ca2+ influx through GluR-B-less AMPA channels leading to non-hebbian forms of plasticity. However, hebbian dependence on simultaneous pre- and postsynaptic activity is often a critical feature for memory storage (reviewed in e.g. [76]); hence, a non-hebbian form of plasticity should result in impaired memorization.\nSurprisingly, in GluR-BΔFB mice no LTP changes could be observed in field measurements in the hippocampus, nor could NMDA-independent LTP be induced in hippocampal synapses between Schaffer collaterals and CA1 pyramidal cells in presence of the NMDA antagonist APV (K. Jensen, O. Hvalby, personal communication). However, in other brain areas that are potentially important for the processing of olfactory information, such as piriform cortex or olfactory bulb, LTP measurements have not yet been performed; synapses of these pathways may be regulated differently than hippocampal CA3/CA1 synapses.\nAdditionally, by changing the Ca2+ permeability of AMPARs, Ca2+ signaling via AMPA and colocalized NMDA channels might be disturbed, thereby impairing memory formation. Other forms of plasticity [77,78] induced by Ca2+-permeable AMPARs might play a prevalent role in olfactory memory. Alternatively, long-term stabilization might involve GluR-B phosphorylation similar to cerebellar long-term depression [79] and thus be selectively impaired by GluR-B depletion. Physiological experiments to assess these hypotheses will ideally make use of even more restricted genetic modifications with completely undisturbed input structures. One possibility would be Cre-mediated GluR-B depletion and GluR-B(Q) expression in piriform cortex as suggested above.\n\nCorrelating Quantitative Behavior and Mosaic Gene Expression for Dissecting Phenotypes\nA critical step in discerning the discrimination and learning phenotypes from the memory phenotype was the observation of increased variability in the memory of the GluR-B knockout animals and, subsequently, the individual analyses of protein expression levels. We made use of the epigenetic variability in GluR-B excision that could be correlated to the variability in memory but showed no correlation to variability in discrimination.\nThe analysis of quantitative trait loci (for review, see [80]), or classically correlating different behavioral phenotypes within a truly wild-type population [81–84], also attempts to find common or distinct genetic origins of different behavioral traits. These attempts undoubtedly contribute significantly to unraveling the molecular basis of behavior. Due to subtle and multigenic differences between different strains of rodents or different individuals in a wild-type population, however, they suffer from a rather low “signal-to-noise” ratio. Differences in individual genes are rather small compared with the vast number of genes involved. As a result, purely correlating behavioral traits within a wild-type population usually remains rather descriptive, whereas quantitative trait loci analysis is capable of revealing multigenic basis of behavioral traits but usually lacks the power to identify the individual genes themselves.\nHerein, we described a way to enhance the signal-to-noise ratio by making use of the mosaic expression often associated with transgenic approaches: combining the advantages of “classical” genetic manipulation—namely, that the target of the manipulation is well defined—with the possibility to analyze variability, might also in future provide novel ways to define molecular and cellular correlates of complex behavioral traits.\nIn this study, we combined genetically induced manipulation of the AMPAR composition with quantitative behavioral and molecular analyses. We could thus provide evidence for opposing roles of specific GluR-B manipulation and increased Ca2+ influx via AMPARs in olfactory discrimination/learning, and memory, potentially in the olfactory bulb and piriform cortex, respectively. To achieve this, we made use of the epigenetic variability in the extent of GluR-B ablation, which correlated with the variability in odor memory, but not in discrimination and learning; this finding was subsequently confirmed in GluR-B rescue mice with piriform cortex-specific transgenic expression of GluR-B. Extending these principles of combining quantitative behavioral analyses with minimal and dosed genetic interference, together with further physiological analyses, will ultimately pinpoint the neural circuitries underlying related, but distinct, behavioral traits in olfactory and other systems."}

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we present mechanistic and spatial dissections of olfactory discrimination, learning, and memory. We employed gene-targeted and transgenic mice with region-specific expression to demonstrate that a change in GluR-B-mediated properties of AMPA channels in αCaMKII-expressing neurons of mouse forebrain, including olfactory bulb mitral and granule cells, enhances olfactory discrimination and learning but impairs olfactory memory. These pertinent olfactory behaviors were assessed in a go/no-go operant conditioning task, which provides a quantitative, robust, and reproducible behavioral tool [3]. We observed among individual mice a striking variability in olfactory memory performance but not in odor discrimination. This variability could be traced to epigenetic variability in the transgenic expression of Cre-recombinase, which mediated recombination within loxP-flanked segments of gene-targeted alleles for the dominant AMPAR subunit GluR-B, and hence operated the switch in AMPAR properties toward GluR-B ablation and increased Ca2+ permeability. In contrast to variable memory, olfactory discrimination and learning performances appeared already saturated by even moderate extents of Cre expression, and hence moderate changes in AMPAR properties. The subsequent transgene-driven re-introduction of GluR-B, specifically in piriform cortex and hippocampus, reversed the Cre-induced loss of GluR-B and partially rescued the odor memory deficit, but left unaltered the enhanced olfactory discrimination. In a nutshell, we conclude that olfactory discrimination is enhanced by an increase in AMPAR-mediated Ca2+ permeability within the olfactory bulb, whereas olfactory memory becomes impaired upon genetically induced GluR-B ablation in higher brain centers, specifically in piriform cortex.\n\nOlfactory Discrimination Is Increased in Mice with Forebrain-Specific GluR-B Ablation or GluR-B(Q) Expression\nBoth forebrain-specific GluR-B(Q) expression and GluR-B depletion led to increased olfactory learning and discrimination capabilities. This was rather pronounced for GluR-B(Q)-expressing mice, consistent with the overall stronger phenotypic consequences in comparison to GluR-B depletion, both when forebrain-selective ([58], and this study) or global [53,60].\nA detailed analysis of the sampling pattern [3], and in particular the analysis of discrimination tasks that involved “simple” dissimilar monomolecular odor pairs and “difficult” binary mixtures, were necessary to fully capture the characteristics of the olfactory discrimination phenotype for forebrain-specific GluR-B-depleted mice. For closely related binary mixtures, discrimination improvements were largest, consistent with a specific alteration in odor discrimination, rather than a general enhancement of learning capabilities. This is further supported by the notion that no general improvement was observed in other nonolfactory behavioral tasks, e.g., hippocampus-dependent spatial learning tasks such as matching-to-place spatial reference memory tasks (Figure S2). As no Cre expression and activity was observed in the main olfactory sensory neurons at any developmental stage (Figure S4 and unpublished data), olfactory epithelial function was unaltered by the genetic modification. The vomeronasal organ showed very weak Cre expression (unpublished data), but a role of this structure concerning performance in the olfactory discrimination task is unlikely (for review, see [63]). The behavioral phenotype is thus likely to be associated with the processing of olfactory information rather than the detection of odors. Furthermore, increased performance even after long stretches of training and, in particular, increased sampling pattern differences (TB and ATS, unpublished data) supported the notion that GluR-B depletion resulted in enhanced odor discrimination capability. The learning phenotype might thus be a result of this enhanced discrimination capability or reflect additional changes in circuits underlying task acquisition.\n\nPutative Cellular Basis of Enhanced Odor Discrimination and Learning\nAMPAR properties were altered specifically in neurons of forebrain areas, most notably olfactory bulb, olfactory cortex, and other cortical areas and hippocampus, leading to enhanced odor discrimination and learning. Interestingly, transgenic expression of GFPGluR-B in GluR-BΔFB mice (genetic “rescue”), specifically in piriform cortex and hippocampus with no detectable expression in the olfactory bulb, did not alter enhanced discrimination and learning capabilities. This is consistent with a primary role of the olfactory bulb in olfactory discrimination and learning. Alternatively, transgenic protein levels might have been too low to alter discrimination and learning capabilities, although memory was clearly affected. This notion will be further tested in mice with piriform cortex-specific GluR-B ablation.\nA direct contribution to the phenotype by Ca2+ influx through genetically modified AMPA channels seems to be likely, since mice expressing Q/R site-unedited GluR-B showed even better odor learning and discrimination performance compared with mice with depleted GluR-B. In both mouse models Ca2+ influx through AMPA channels is increased, whereas the effect on the macroscopic AMPA conductance differs. AMPAR currents are reduced in mice not expressing GluR-B [51], possibly due to fewer synaptic AMPA channels and impaired AMPAR trafficking and recycling. In mice expressing the unedited form of GluR-B(Q), macroscopic conductance in whole-cell patches of CA1 pyramidals is increased [60], but excitatory transmission in CA3-to-CA1 cell synapses is somewhat reduced, in spite of a lower threshold for generating a population spike [58], indicating increased synaptic excitability by sustained GluR-B(Q) expression, in line with the seizure-prone phenotype. Yet, both mouse models yield enhanced discrimination and learning capability. The milder phenotype upon GluR-B depletion could be attributed to reduced AMPAR densities at synapses [40,41] and therefore probably to a lesser extent of Ca2+ influx. This is further supported by kainate-induced Co2+ uptake in acute brain slices, revealing considerably higher Co2+ uptake via Ca2+-permeable AMPARs in hippocampal pyramidal neurons of mice expressing GluR-B(Q), than those lacking GluR-B (DRS, RS, and PHS, unpublished data).\nNormally, GluR-B-containing AMPARs are prominently localized at the dendrodendritic synapse between mitral and granule cells in the olfactory bulb [64,65]. As Ca2+ influx through glutamate receptors is thought to contribute to lateral and recurrent inhibition ([38] see also [39]), the absence of GluR-B, or the presence of GluR-B(Q) in the olfactory bulb, is likely to result in increased inhibition between the principal neurons in this structure. Notably, the improved olfactory discrimination capabilities were apparent even upon relatively small reductions in GluR-B levels. It will be interesting to see if GluR-B+/neo mice also exhibit enhanced odor discrimination, which is indeed likely given that low levels of GluR-B(Q), and hence a small increase in Ca2+-permeable AMPARs, arise from the attenuated GluR-Bneo allele [60], and, moreover, that GluR-B levels are decreased in these mice due to the single copy of the GluR-B+ allele.\nIn virtually all models of the olfactory bulb, lateral (and, in fewer models, also recurrent) inhibition plays a dominant role, either in establishing spatiotemporal dynamics [32,66–69], or in directly enhancing contrast and therefore simplifying discrimination and learning of similar odorants [24,28,29,36]. Increased inhibition will thus in general improve discriminability, consistent with the behavioral improvements observed with GluR-B(Q) expression, the GluR-B knockout, and the “rescue” mice. A direct test of this link would require the quantitative measurement of inhibition in the intact preparation, a task that might be feasible with further improved in vivo electrophysiological techniques, such as targeted recordings [70,71] or simultaneous pre- and postsynaptic intracellular measurements.\n\nOlfactory Memory Is Reduced in GluR-B Knockout Mice and Improved by GluR-B Expression in Piriform Cortex and Hippocampus\nTo assess olfactory memory of GluR-BΔFB mice, after six days the mice were probed with unrewarded odor presentations that interleaved a simple discrimination task. Prolonged behavioral tasks such as the assessment of long-term olfactory memory were not performed with the seizure-prone GluR-BΔECS:FB mice. Memory in GluR-BΔFB mice, however, was dramatically impaired. This cannot be attributed to a general, unspecific deficit because, simultaneous to the memory trials, the normal, rewarded discrimination task was performed even better than by controls. Reduced olfactory memory can also not be simply attributed to increased extinction, as no significant trial-group interactions were observed and also, when restricted to the first unrewarded memory trials, a significant impairment was observed (Figure S3A). Additionally, investigating relearning of the first discrimination task revealed a significant correlation with the memory performance, showing a “memory” deficit under extinction-free conditions (Figure S3B). Finally, in other memory-related tasks, such as a hippocampus-dependent spatial reference memory task (Figure S2), mice with GluR-B depletion were not impaired after task acquisition. We therefore conclude that forebrain-specific ablation of GluR-B results in a specific loss of long-term olfactory memory but, at the same time, in enhanced odor discrimination and learning capabilities.\nTo dissect the discrimination, learning, and memory phenotypes, and ultimately identify potential cellular correlates, we made use of the variegated Cre expression of TgCre4 mice. Therefore, residual GluR-B levels were determined from each mouse that had been tested in the behavioral experiments, and levels were correlated with odor learning, discrimination, and olfactory memory. The significant direct correlation between residual GluR-B levels in hippocampus and cortical areas with olfactory memory suggested hippocampal and/or cortical neurons as putative mediators for odor memorization and/or storage. No measure of discrimination and learning, on the other hand, correlated with residual GluR-B levels; even the smallest reduction in GluR-B levels (about 20%–60%) was sufficient to establish and saturate enhanced odor discrimination capabilities. Together, this allows the conclusion that distinct mechanisms mediate discrimination/learning and memory. This is furthermore consistent with a prominent role of cortical areas or hippocampus in olfactory memory, although GluR-B levels in the olfactory bulb were also weakly correlated with memory performance. Transgenic expression of GFPGluR-B in piriform cortex and hippocampus indeed rescued memory to an extent strikingly consistent with the transgenic protein levels (approximately 10% of wild-type GluR-B), confirming the reliability of the correlation analysis and the sensitivity of the behavioral assay.\nIn general, the hippocampus is thought to be involved in only those olfactory memory tasks that involve temporal sequence analysis or require other higher cognitive features [2,13,72–74]. In particular, extensive lesions to the hippocampal formation in rats do not interfere with long-term olfactory memory in go/no-go successive olfactory discrimination tasks [72], such as the one described. This leaves piriform cortex as the most prominent candidate for the locus of the olfactory memory deficit described, consistent with the prevalent view of piriform cortex as an associational memory structure [75] and learning-associated changes in piriform cortex [7,20–23].\n\nPotential Mechanisms of Specific Olfactory Memory Impairment\nWhat could be the cellular basis of the long-term memory deficit brought about by lack of GluR-B-containing AMPARs? For complete GluR-B knockouts, increased long-term plasticity (LTP) was reported in hippocampal field recordings [51]. In addition, in hippocampal and amygdala pathways lacking GluR-B, an AMPAR-dependent, N-methyl-D-aspartate (NMDA) receptor-independent form of LTP can be readily induced [51,52]. Mechanistically, this is likely to be due to Ca2+ influx through GluR-B-less AMPA channels leading to non-hebbian forms of plasticity. However, hebbian dependence on simultaneous pre- and postsynaptic activity is often a critical feature for memory storage (reviewed in e.g. [76]); hence, a non-hebbian form of plasticity should result in impaired memorization.\nSurprisingly, in GluR-BΔFB mice no LTP changes could be observed in field measurements in the hippocampus, nor could NMDA-independent LTP be induced in hippocampal synapses between Schaffer collaterals and CA1 pyramidal cells in presence of the NMDA antagonist APV (K. Jensen, O. Hvalby, personal communication). However, in other brain areas that are potentially important for the processing of olfactory information, such as piriform cortex or olfactory bulb, LTP measurements have not yet been performed; synapses of these pathways may be regulated differently than hippocampal CA3/CA1 synapses.\nAdditionally, by changing the Ca2+ permeability of AMPARs, Ca2+ signaling via AMPA and colocalized NMDA channels might be disturbed, thereby impairing memory formation. Other forms of plasticity [77,78] induced by Ca2+-permeable AMPARs might play a prevalent role in olfactory memory. Alternatively, long-term stabilization might involve GluR-B phosphorylation similar to cerebellar long-term depression [79] and thus be selectively impaired by GluR-B depletion. Physiological experiments to assess these hypotheses will ideally make use of even more restricted genetic modifications with completely undisturbed input structures. One possibility would be Cre-mediated GluR-B depletion and GluR-B(Q) expression in piriform cortex as suggested above.\n\nCorrelating Quantitative Behavior and Mosaic Gene Expression for Dissecting Phenotypes\nA critical step in discerning the discrimination and learning phenotypes from the memory phenotype was the observation of increased variability in the memory of the GluR-B knockout animals and, subsequently, the individual analyses of protein expression levels. We made use of the epigenetic variability in GluR-B excision that could be correlated to the variability in memory but showed no correlation to variability in discrimination.\nThe analysis of quantitative trait loci (for review, see [80]), or classically correlating different behavioral phenotypes within a truly wild-type population [81–84], also attempts to find common or distinct genetic origins of different behavioral traits. These attempts undoubtedly contribute significantly to unraveling the molecular basis of behavior. Due to subtle and multigenic differences between different strains of rodents or different individuals in a wild-type population, however, they suffer from a rather low “signal-to-noise” ratio. Differences in individual genes are rather small compared with the vast number of genes involved. As a result, purely correlating behavioral traits within a wild-type population usually remains rather descriptive, whereas quantitative trait loci analysis is capable of revealing multigenic basis of behavioral traits but usually lacks the power to identify the individual genes themselves.\nHerein, we described a way to enhance the signal-to-noise ratio by making use of the mosaic expression often associated with transgenic approaches: combining the advantages of “classical” genetic manipulation—namely, that the target of the manipulation is well defined—with the possibility to analyze variability, might also in future provide novel ways to define molecular and cellular correlates of complex behavioral traits.\nIn this study, we combined genetically induced manipulation of the AMPAR composition with quantitative behavioral and molecular analyses. We could thus provide evidence for opposing roles of specific GluR-B manipulation and increased Ca2+ influx via AMPARs in olfactory discrimination/learning, and memory, potentially in the olfactory bulb and piriform cortex, respectively. To achieve this, we made use of the epigenetic variability in the extent of GluR-B ablation, which correlated with the variability in odor memory, but not in discrimination and learning; this finding was subsequently confirmed in GluR-B rescue mice with piriform cortex-specific transgenic expression of GluR-B. Extending these principles of combining quantitative behavioral analyses with minimal and dosed genetic interference, together with further physiological analyses, will ultimately pinpoint the neural circuitries underlying related, but distinct, behavioral traits in olfactory and other systems."}

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we present mechanistic and spatial dissections of olfactory discrimination, learning, and memory. We employed gene-targeted and transgenic mice with region-specific expression to demonstrate that a change in GluR-B-mediated properties of AMPA channels in αCaMKII-expressing neurons of mouse forebrain, including olfactory bulb mitral and granule cells, enhances olfactory discrimination and learning but impairs olfactory memory. These pertinent olfactory behaviors were assessed in a go/no-go operant conditioning task, which provides a quantitative, robust, and reproducible behavioral tool [3]. We observed among individual mice a striking variability in olfactory memory performance but not in odor discrimination. This variability could be traced to epigenetic variability in the transgenic expression of Cre-recombinase, which mediated recombination within loxP-flanked segments of gene-targeted alleles for the dominant AMPAR subunit GluR-B, and hence operated the switch in AMPAR properties toward GluR-B ablation and increased Ca2+ permeability. In contrast to variable memory, olfactory discrimination and learning performances appeared already saturated by even moderate extents of Cre expression, and hence moderate changes in AMPAR properties. The subsequent transgene-driven re-introduction of GluR-B, specifically in piriform cortex and hippocampus, reversed the Cre-induced loss of GluR-B and partially rescued the odor memory deficit, but left unaltered the enhanced olfactory discrimination. In a nutshell, we conclude that olfactory discrimination is enhanced by an increase in AMPAR-mediated Ca2+ permeability within the olfactory bulb, whereas olfactory memory becomes impaired upon genetically induced GluR-B ablation in higher brain centers, specifically in piriform cortex.\n\nOlfactory Discrimination Is Increased in Mice with Forebrain-Specific GluR-B Ablation or GluR-B(Q) Expression\nBoth forebrain-specific GluR-B(Q) expression and GluR-B depletion led to increased olfactory learning and discrimination capabilities. This was rather pronounced for GluR-B(Q)-expressing mice, consistent with the overall stronger phenotypic consequences in comparison to GluR-B depletion, both when forebrain-selective ([58], and this study) or global [53,60].\nA detailed analysis of the sampling pattern [3], and in particular the analysis of discrimination tasks that involved “simple” dissimilar monomolecular odor pairs and “difficult” binary mixtures, were necessary to fully capture the characteristics of the olfactory discrimination phenotype for forebrain-specific GluR-B-depleted mice. For closely related binary mixtures, discrimination improvements were largest, consistent with a specific alteration in odor discrimination, rather than a general enhancement of learning capabilities. This is further supported by the notion that no general improvement was observed in other nonolfactory behavioral tasks, e.g., hippocampus-dependent spatial learning tasks such as matching-to-place spatial reference memory tasks (Figure S2). As no Cre expression and activity was observed in the main olfactory sensory neurons at any developmental stage (Figure S4 and unpublished data), olfactory epithelial function was unaltered by the genetic modification. The vomeronasal organ showed very weak Cre expression (unpublished data), but a role of this structure concerning performance in the olfactory discrimination task is unlikely (for review, see [63]). The behavioral phenotype is thus likely to be associated with the processing of olfactory information rather than the detection of odors. Furthermore, increased performance even after long stretches of training and, in particular, increased sampling pattern differences (TB and ATS, unpublished data) supported the notion that GluR-B depletion resulted in enhanced odor discrimination capability. The learning phenotype might thus be a result of this enhanced discrimination capability or reflect additional changes in circuits underlying task acquisition.\n\nPutative Cellular Basis of Enhanced Odor Discrimination and Learning\nAMPAR properties were altered specifically in neurons of forebrain areas, most notably olfactory bulb, olfactory cortex, and other cortical areas and hippocampus, leading to enhanced odor discrimination and learning. Interestingly, transgenic expression of GFPGluR-B in GluR-BΔFB mice (genetic “rescue”), specifically in piriform cortex and hippocampus with no detectable expression in the olfactory bulb, did not alter enhanced discrimination and learning capabilities. This is consistent with a primary role of the olfactory bulb in olfactory discrimination and learning. Alternatively, transgenic protein levels might have been too low to alter discrimination and learning capabilities, although memory was clearly affected. This notion will be further tested in mice with piriform cortex-specific GluR-B ablation.\nA direct contribution to the phenotype by Ca2+ influx through genetically modified AMPA channels seems to be likely, since mice expressing Q/R site-unedited GluR-B showed even better odor learning and discrimination performance compared with mice with depleted GluR-B. In both mouse models Ca2+ influx through AMPA channels is increased, whereas the effect on the macroscopic AMPA conductance differs. AMPAR currents are reduced in mice not expressing GluR-B [51], possibly due to fewer synaptic AMPA channels and impaired AMPAR trafficking and recycling. In mice expressing the unedited form of GluR-B(Q), macroscopic conductance in whole-cell patches of CA1 pyramidals is increased [60], but excitatory transmission in CA3-to-CA1 cell synapses is somewhat reduced, in spite of a lower threshold for generating a population spike [58], indicating increased synaptic excitability by sustained GluR-B(Q) expression, in line with the seizure-prone phenotype. Yet, both mouse models yield enhanced discrimination and learning capability. The milder phenotype upon GluR-B depletion could be attributed to reduced AMPAR densities at synapses [40,41] and therefore probably to a lesser extent of Ca2+ influx. This is further supported by kainate-induced Co2+ uptake in acute brain slices, revealing considerably higher Co2+ uptake via Ca2+-permeable AMPARs in hippocampal pyramidal neurons of mice expressing GluR-B(Q), than those lacking GluR-B (DRS, RS, and PHS, unpublished data).\nNormally, GluR-B-containing AMPARs are prominently localized at the dendrodendritic synapse between mitral and granule cells in the olfactory bulb [64,65]. As Ca2+ influx through glutamate receptors is thought to contribute to lateral and recurrent inhibition ([38] see also [39]), the absence of GluR-B, or the presence of GluR-B(Q) in the olfactory bulb, is likely to result in increased inhibition between the principal neurons in this structure. Notably, the improved olfactory discrimination capabilities were apparent even upon relatively small reductions in GluR-B levels. It will be interesting to see if GluR-B+/neo mice also exhibit enhanced odor discrimination, which is indeed likely given that low levels of GluR-B(Q), and hence a small increase in Ca2+-permeable AMPARs, arise from the attenuated GluR-Bneo allele [60], and, moreover, that GluR-B levels are decreased in these mice due to the single copy of the GluR-B+ allele.\nIn virtually all models of the olfactory bulb, lateral (and, in fewer models, also recurrent) inhibition plays a dominant role, either in establishing spatiotemporal dynamics [32,66–69], or in directly enhancing contrast and therefore simplifying discrimination and learning of similar odorants [24,28,29,36]. Increased inhibition will thus in general improve discriminability, consistent with the behavioral improvements observed with GluR-B(Q) expression, the GluR-B knockout, and the “rescue” mice. A direct test of this link would require the quantitative measurement of inhibition in the intact preparation, a task that might be feasible with further improved in vivo electrophysiological techniques, such as targeted recordings [70,71] or simultaneous pre- and postsynaptic intracellular measurements.\n\nOlfactory Memory Is Reduced in GluR-B Knockout Mice and Improved by GluR-B Expression in Piriform Cortex and Hippocampus\nTo assess olfactory memory of GluR-BΔFB mice, after six days the mice were probed with unrewarded odor presentations that interleaved a simple discrimination task. Prolonged behavioral tasks such as the assessment of long-term olfactory memory were not performed with the seizure-prone GluR-BΔECS:FB mice. Memory in GluR-BΔFB mice, however, was dramatically impaired. This cannot be attributed to a general, unspecific deficit because, simultaneous to the memory trials, the normal, rewarded discrimination task was performed even better than by controls. Reduced olfactory memory can also not be simply attributed to increased extinction, as no significant trial-group interactions were observed and also, when restricted to the first unrewarded memory trials, a significant impairment was observed (Figure S3A). Additionally, investigating relearning of the first discrimination task revealed a significant correlation with the memory performance, showing a “memory” deficit under extinction-free conditions (Figure S3B). Finally, in other memory-related tasks, such as a hippocampus-dependent spatial reference memory task (Figure S2), mice with GluR-B depletion were not impaired after task acquisition. We therefore conclude that forebrain-specific ablation of GluR-B results in a specific loss of long-term olfactory memory but, at the same time, in enhanced odor discrimination and learning capabilities.\nTo dissect the discrimination, learning, and memory phenotypes, and ultimately identify potential cellular correlates, we made use of the variegated Cre expression of TgCre4 mice. Therefore, residual GluR-B levels were determined from each mouse that had been tested in the behavioral experiments, and levels were correlated with odor learning, discrimination, and olfactory memory. The significant direct correlation between residual GluR-B levels in hippocampus and cortical areas with olfactory memory suggested hippocampal and/or cortical neurons as putative mediators for odor memorization and/or storage. No measure of discrimination and learning, on the other hand, correlated with residual GluR-B levels; even the smallest reduction in GluR-B levels (about 20%–60%) was sufficient to establish and saturate enhanced odor discrimination capabilities. Together, this allows the conclusion that distinct mechanisms mediate discrimination/learning and memory. This is furthermore consistent with a prominent role of cortical areas or hippocampus in olfactory memory, although GluR-B levels in the olfactory bulb were also weakly correlated with memory performance. Transgenic expression of GFPGluR-B in piriform cortex and hippocampus indeed rescued memory to an extent strikingly consistent with the transgenic protein levels (approximately 10% of wild-type GluR-B), confirming the reliability of the correlation analysis and the sensitivity of the behavioral assay.\nIn general, the hippocampus is thought to be involved in only those olfactory memory tasks that involve temporal sequence analysis or require other higher cognitive features [2,13,72–74]. In particular, extensive lesions to the hippocampal formation in rats do not interfere with long-term olfactory memory in go/no-go successive olfactory discrimination tasks [72], such as the one described. This leaves piriform cortex as the most prominent candidate for the locus of the olfactory memory deficit described, consistent with the prevalent view of piriform cortex as an associational memory structure [75] and learning-associated changes in piriform cortex [7,20–23].\n\nPotential Mechanisms of Specific Olfactory Memory Impairment\nWhat could be the cellular basis of the long-term memory deficit brought about by lack of GluR-B-containing AMPARs? For complete GluR-B knockouts, increased long-term plasticity (LTP) was reported in hippocampal field recordings [51]. In addition, in hippocampal and amygdala pathways lacking GluR-B, an AMPAR-dependent, N-methyl-D-aspartate (NMDA) receptor-independent form of LTP can be readily induced [51,52]. Mechanistically, this is likely to be due to Ca2+ influx through GluR-B-less AMPA channels leading to non-hebbian forms of plasticity. However, hebbian dependence on simultaneous pre- and postsynaptic activity is often a critical feature for memory storage (reviewed in e.g. [76]); hence, a non-hebbian form of plasticity should result in impaired memorization.\nSurprisingly, in GluR-BΔFB mice no LTP changes could be observed in field measurements in the hippocampus, nor could NMDA-independent LTP be induced in hippocampal synapses between Schaffer collaterals and CA1 pyramidal cells in presence of the NMDA antagonist APV (K. Jensen, O. Hvalby, personal communication). However, in other brain areas that are potentially important for the processing of olfactory information, such as piriform cortex or olfactory bulb, LTP measurements have not yet been performed; synapses of these pathways may be regulated differently than hippocampal CA3/CA1 synapses.\nAdditionally, by changing the Ca2+ permeability of AMPARs, Ca2+ signaling via AMPA and colocalized NMDA channels might be disturbed, thereby impairing memory formation. Other forms of plasticity [77,78] induced by Ca2+-permeable AMPARs might play a prevalent role in olfactory memory. Alternatively, long-term stabilization might involve GluR-B phosphorylation similar to cerebellar long-term depression [79] and thus be selectively impaired by GluR-B depletion. Physiological experiments to assess these hypotheses will ideally make use of even more restricted genetic modifications with completely undisturbed input structures. One possibility would be Cre-mediated GluR-B depletion and GluR-B(Q) expression in piriform cortex as suggested above.\n\nCorrelating Quantitative Behavior and Mosaic Gene Expression for Dissecting Phenotypes\nA critical step in discerning the discrimination and learning phenotypes from the memory phenotype was the observation of increased variability in the memory of the GluR-B knockout animals and, subsequently, the individual analyses of protein expression levels. We made use of the epigenetic variability in GluR-B excision that could be correlated to the variability in memory but showed no correlation to variability in discrimination.\nThe analysis of quantitative trait loci (for review, see [80]), or classically correlating different behavioral phenotypes within a truly wild-type population [81–84], also attempts to find common or distinct genetic origins of different behavioral traits. These attempts undoubtedly contribute significantly to unraveling the molecular basis of behavior. Due to subtle and multigenic differences between different strains of rodents or different individuals in a wild-type population, however, they suffer from a rather low “signal-to-noise” ratio. Differences in individual genes are rather small compared with the vast number of genes involved. As a result, purely correlating behavioral traits within a wild-type population usually remains rather descriptive, whereas quantitative trait loci analysis is capable of revealing multigenic basis of behavioral traits but usually lacks the power to identify the individual genes themselves.\nHerein, we described a way to enhance the signal-to-noise ratio by making use of the mosaic expression often associated with transgenic approaches: combining the advantages of “classical” genetic manipulation—namely, that the target of the manipulation is well defined—with the possibility to analyze variability, might also in future provide novel ways to define molecular and cellular correlates of complex behavioral traits.\nIn this study, we combined genetically induced manipulation of the AMPAR composition with quantitative behavioral and molecular analyses. We could thus provide evidence for opposing roles of specific GluR-B manipulation and increased Ca2+ influx via AMPARs in olfactory discrimination/learning, and memory, potentially in the olfactory bulb and piriform cortex, respectively. To achieve this, we made use of the epigenetic variability in the extent of GluR-B ablation, which correlated with the variability in odor memory, but not in discrimination and learning; this finding was subsequently confirmed in GluR-B rescue mice with piriform cortex-specific transgenic expression of GluR-B. Extending these principles of combining quantitative behavioral analyses with minimal and dosed genetic interference, together with further physiological analyses, will ultimately pinpoint the neural circuitries underlying related, but distinct, behavioral traits in olfactory and other systems."}

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we present mechanistic and spatial dissections of olfactory discrimination, learning, and memory. We employed gene-targeted and transgenic mice with region-specific expression to demonstrate that a change in GluR-B-mediated properties of AMPA channels in αCaMKII-expressing neurons of mouse forebrain, including olfactory bulb mitral and granule cells, enhances olfactory discrimination and learning but impairs olfactory memory. These pertinent olfactory behaviors were assessed in a go/no-go operant conditioning task, which provides a quantitative, robust, and reproducible behavioral tool [3]. We observed among individual mice a striking variability in olfactory memory performance but not in odor discrimination. This variability could be traced to epigenetic variability in the transgenic expression of Cre-recombinase, which mediated recombination within loxP-flanked segments of gene-targeted alleles for the dominant AMPAR subunit GluR-B, and hence operated the switch in AMPAR properties toward GluR-B ablation and increased Ca2+ permeability. In contrast to variable memory, olfactory discrimination and learning performances appeared already saturated by even moderate extents of Cre expression, and hence moderate changes in AMPAR properties. The subsequent transgene-driven re-introduction of GluR-B, specifically in piriform cortex and hippocampus, reversed the Cre-induced loss of GluR-B and partially rescued the odor memory deficit, but left unaltered the enhanced olfactory discrimination. In a nutshell, we conclude that olfactory discrimination is enhanced by an increase in AMPAR-mediated Ca2+ permeability within the olfactory bulb, whereas olfactory memory becomes impaired upon genetically induced GluR-B ablation in higher brain centers, specifically in piriform cortex.\n\nOlfactory Discrimination Is Increased in Mice with Forebrain-Specific GluR-B Ablation or GluR-B(Q) Expression\nBoth forebrain-specific GluR-B(Q) expression and GluR-B depletion led to increased olfactory learning and discrimination capabilities. This was rather pronounced for GluR-B(Q)-expressing mice, consistent with the overall stronger phenotypic consequences in comparison to GluR-B depletion, both when forebrain-selective ([58], and this study) or global [53,60].\nA detailed analysis of the sampling pattern [3], and in particular the analysis of discrimination tasks that involved “simple” dissimilar monomolecular odor pairs and “difficult” binary mixtures, were necessary to fully capture the characteristics of the olfactory discrimination phenotype for forebrain-specific GluR-B-depleted mice. For closely related binary mixtures, discrimination improvements were largest, consistent with a specific alteration in odor discrimination, rather than a general enhancement of learning capabilities. This is further supported by the notion that no general improvement was observed in other nonolfactory behavioral tasks, e.g., hippocampus-dependent spatial learning tasks such as matching-to-place spatial reference memory tasks (Figure S2). As no Cre expression and activity was observed in the main olfactory sensory neurons at any developmental stage (Figure S4 and unpublished data), olfactory epithelial function was unaltered by the genetic modification. The vomeronasal organ showed very weak Cre expression (unpublished data), but a role of this structure concerning performance in the olfactory discrimination task is unlikely (for review, see [63]). The behavioral phenotype is thus likely to be associated with the processing of olfactory information rather than the detection of odors. Furthermore, increased performance even after long stretches of training and, in particular, increased sampling pattern differences (TB and ATS, unpublished data) supported the notion that GluR-B depletion resulted in enhanced odor discrimination capability. The learning phenotype might thus be a result of this enhanced discrimination capability or reflect additional changes in circuits underlying task acquisition.\n\nPutative Cellular Basis of Enhanced Odor Discrimination and Learning\nAMPAR properties were altered specifically in neurons of forebrain areas, most notably olfactory bulb, olfactory cortex, and other cortical areas and hippocampus, leading to enhanced odor discrimination and learning. Interestingly, transgenic expression of GFPGluR-B in GluR-BΔFB mice (genetic “rescue”), specifically in piriform cortex and hippocampus with no detectable expression in the olfactory bulb, did not alter enhanced discrimination and learning capabilities. This is consistent with a primary role of the olfactory bulb in olfactory discrimination and learning. Alternatively, transgenic protein levels might have been too low to alter discrimination and learning capabilities, although memory was clearly affected. This notion will be further tested in mice with piriform cortex-specific GluR-B ablation.\nA direct contribution to the phenotype by Ca2+ influx through genetically modified AMPA channels seems to be likely, since mice expressing Q/R site-unedited GluR-B showed even better odor learning and discrimination performance compared with mice with depleted GluR-B. In both mouse models Ca2+ influx through AMPA channels is increased, whereas the effect on the macroscopic AMPA conductance differs. AMPAR currents are reduced in mice not expressing GluR-B [51], possibly due to fewer synaptic AMPA channels and impaired AMPAR trafficking and recycling. In mice expressing the unedited form of GluR-B(Q), macroscopic conductance in whole-cell patches of CA1 pyramidals is increased [60], but excitatory transmission in CA3-to-CA1 cell synapses is somewhat reduced, in spite of a lower threshold for generating a population spike [58], indicating increased synaptic excitability by sustained GluR-B(Q) expression, in line with the seizure-prone phenotype. Yet, both mouse models yield enhanced discrimination and learning capability. The milder phenotype upon GluR-B depletion could be attributed to reduced AMPAR densities at synapses [40,41] and therefore probably to a lesser extent of Ca2+ influx. This is further supported by kainate-induced Co2+ uptake in acute brain slices, revealing considerably higher Co2+ uptake via Ca2+-permeable AMPARs in hippocampal pyramidal neurons of mice expressing GluR-B(Q), than those lacking GluR-B (DRS, RS, and PHS, unpublished data).\nNormally, GluR-B-containing AMPARs are prominently localized at the dendrodendritic synapse between mitral and granule cells in the olfactory bulb [64,65]. As Ca2+ influx through glutamate receptors is thought to contribute to lateral and recurrent inhibition ([38] see also [39]), the absence of GluR-B, or the presence of GluR-B(Q) in the olfactory bulb, is likely to result in increased inhibition between the principal neurons in this structure. Notably, the improved olfactory discrimination capabilities were apparent even upon relatively small reductions in GluR-B levels. It will be interesting to see if GluR-B+/neo mice also exhibit enhanced odor discrimination, which is indeed likely given that low levels of GluR-B(Q), and hence a small increase in Ca2+-permeable AMPARs, arise from the attenuated GluR-Bneo allele [60], and, moreover, that GluR-B levels are decreased in these mice due to the single copy of the GluR-B+ allele.\nIn virtually all models of the olfactory bulb, lateral (and, in fewer models, also recurrent) inhibition plays a dominant role, either in establishing spatiotemporal dynamics [32,66–69], or in directly enhancing contrast and therefore simplifying discrimination and learning of similar odorants [24,28,29,36]. Increased inhibition will thus in general improve discriminability, consistent with the behavioral improvements observed with GluR-B(Q) expression, the GluR-B knockout, and the “rescue” mice. A direct test of this link would require the quantitative measurement of inhibition in the intact preparation, a task that might be feasible with further improved in vivo electrophysiological techniques, such as targeted recordings [70,71] or simultaneous pre- and postsynaptic intracellular measurements.\n\nOlfactory Memory Is Reduced in GluR-B Knockout Mice and Improved by GluR-B Expression in Piriform Cortex and Hippocampus\nTo assess olfactory memory of GluR-BΔFB mice, after six days the mice were probed with unrewarded odor presentations that interleaved a simple discrimination task. Prolonged behavioral tasks such as the assessment of long-term olfactory memory were not performed with the seizure-prone GluR-BΔECS:FB mice. Memory in GluR-BΔFB mice, however, was dramatically impaired. This cannot be attributed to a general, unspecific deficit because, simultaneous to the memory trials, the normal, rewarded discrimination task was performed even better than by controls. Reduced olfactory memory can also not be simply attributed to increased extinction, as no significant trial-group interactions were observed and also, when restricted to the first unrewarded memory trials, a significant impairment was observed (Figure S3A). Additionally, investigating relearning of the first discrimination task revealed a significant correlation with the memory performance, showing a “memory” deficit under extinction-free conditions (Figure S3B). Finally, in other memory-related tasks, such as a hippocampus-dependent spatial reference memory task (Figure S2), mice with GluR-B depletion were not impaired after task acquisition. We therefore conclude that forebrain-specific ablation of GluR-B results in a specific loss of long-term olfactory memory but, at the same time, in enhanced odor discrimination and learning capabilities.\nTo dissect the discrimination, learning, and memory phenotypes, and ultimately identify potential cellular correlates, we made use of the variegated Cre expression of TgCre4 mice. Therefore, residual GluR-B levels were determined from each mouse that had been tested in the behavioral experiments, and levels were correlated with odor learning, discrimination, and olfactory memory. The significant direct correlation between residual GluR-B levels in hippocampus and cortical areas with olfactory memory suggested hippocampal and/or cortical neurons as putative mediators for odor memorization and/or storage. No measure of discrimination and learning, on the other hand, correlated with residual GluR-B levels; even the smallest reduction in GluR-B levels (about 20%–60%) was sufficient to establish and saturate enhanced odor discrimination capabilities. Together, this allows the conclusion that distinct mechanisms mediate discrimination/learning and memory. This is furthermore consistent with a prominent role of cortical areas or hippocampus in olfactory memory, although GluR-B levels in the olfactory bulb were also weakly correlated with memory performance. Transgenic expression of GFPGluR-B in piriform cortex and hippocampus indeed rescued memory to an extent strikingly consistent with the transgenic protein levels (approximately 10% of wild-type GluR-B), confirming the reliability of the correlation analysis and the sensitivity of the behavioral assay.\nIn general, the hippocampus is thought to be involved in only those olfactory memory tasks that involve temporal sequence analysis or require other higher cognitive features [2,13,72–74]. In particular, extensive lesions to the hippocampal formation in rats do not interfere with long-term olfactory memory in go/no-go successive olfactory discrimination tasks [72], such as the one described. This leaves piriform cortex as the most prominent candidate for the locus of the olfactory memory deficit described, consistent with the prevalent view of piriform cortex as an associational memory structure [75] and learning-associated changes in piriform cortex [7,20–23].\n\nPotential Mechanisms of Specific Olfactory Memory Impairment\nWhat could be the cellular basis of the long-term memory deficit brought about by lack of GluR-B-containing AMPARs? For complete GluR-B knockouts, increased long-term plasticity (LTP) was reported in hippocampal field recordings [51]. In addition, in hippocampal and amygdala pathways lacking GluR-B, an AMPAR-dependent, N-methyl-D-aspartate (NMDA) receptor-independent form of LTP can be readily induced [51,52]. Mechanistically, this is likely to be due to Ca2+ influx through GluR-B-less AMPA channels leading to non-hebbian forms of plasticity. However, hebbian dependence on simultaneous pre- and postsynaptic activity is often a critical feature for memory storage (reviewed in e.g. [76]); hence, a non-hebbian form of plasticity should result in impaired memorization.\nSurprisingly, in GluR-BΔFB mice no LTP changes could be observed in field measurements in the hippocampus, nor could NMDA-independent LTP be induced in hippocampal synapses between Schaffer collaterals and CA1 pyramidal cells in presence of the NMDA antagonist APV (K. Jensen, O. Hvalby, personal communication). However, in other brain areas that are potentially important for the processing of olfactory information, such as piriform cortex or olfactory bulb, LTP measurements have not yet been performed; synapses of these pathways may be regulated differently than hippocampal CA3/CA1 synapses.\nAdditionally, by changing the Ca2+ permeability of AMPARs, Ca2+ signaling via AMPA and colocalized NMDA channels might be disturbed, thereby impairing memory formation. Other forms of plasticity [77,78] induced by Ca2+-permeable AMPARs might play a prevalent role in olfactory memory. Alternatively, long-term stabilization might involve GluR-B phosphorylation similar to cerebellar long-term depression [79] and thus be selectively impaired by GluR-B depletion. Physiological experiments to assess these hypotheses will ideally make use of even more restricted genetic modifications with completely undisturbed input structures. One possibility would be Cre-mediated GluR-B depletion and GluR-B(Q) expression in piriform cortex as suggested above.\n\nCorrelating Quantitative Behavior and Mosaic Gene Expression for Dissecting Phenotypes\nA critical step in discerning the discrimination and learning phenotypes from the memory phenotype was the observation of increased variability in the memory of the GluR-B knockout animals and, subsequently, the individual analyses of protein expression levels. We made use of the epigenetic variability in GluR-B excision that could be correlated to the variability in memory but showed no correlation to variability in discrimination.\nThe analysis of quantitative trait loci (for review, see [80]), or classically correlating different behavioral phenotypes within a truly wild-type population [81–84], also attempts to find common or distinct genetic origins of different behavioral traits. These attempts undoubtedly contribute significantly to unraveling the molecular basis of behavior. Due to subtle and multigenic differences between different strains of rodents or different individuals in a wild-type population, however, they suffer from a rather low “signal-to-noise” ratio. Differences in individual genes are rather small compared with the vast number of genes involved. As a result, purely correlating behavioral traits within a wild-type population usually remains rather descriptive, whereas quantitative trait loci analysis is capable of revealing multigenic basis of behavioral traits but usually lacks the power to identify the individual genes themselves.\nHerein, we described a way to enhance the signal-to-noise ratio by making use of the mosaic expression often associated with transgenic approaches: combining the advantages of “classical” genetic manipulation—namely, that the target of the manipulation is well defined—with the possibility to analyze variability, might also in future provide novel ways to define molecular and cellular correlates of complex behavioral traits.\nIn this study, we combined genetically induced manipulation of the AMPAR composition with quantitative behavioral and molecular analyses. We could thus provide evidence for opposing roles of specific GluR-B manipulation and increased Ca2+ influx via AMPARs in olfactory discrimination/learning, and memory, potentially in the olfactory bulb and piriform cortex, respectively. To achieve this, we made use of the epigenetic variability in the extent of GluR-B ablation, which correlated with the variability in odor memory, but not in discrimination and learning; this finding was subsequently confirmed in GluR-B rescue mice with piriform cortex-specific transgenic expression of GluR-B. Extending these principles of combining quantitative behavioral analyses with minimal and dosed genetic interference, together with further physiological analyses, will ultimately pinpoint the neural circuitries underlying related, but distinct, behavioral traits in olfactory and other systems."}