Limits...
Profound context-dependent plasticity of mitral cell responses in olfactory bulb.

Doucette W, Restrepo D - PLoS Biol. (2008)

Bottom Line: The response changes occur in a manner that increases the ability of the circuit to convey information necessary to discriminate among closely related odors.Remarkably, a switch between which of the two odors is rewarded causes mitral cells to switch the polarity of their divergent responses.Taken together these results redefine the function of the OB as a transiently modifiable (active) filter, shaping early odor representations in behaviorally meaningful ways.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Developmental Biology, Neuroscience Program, Rocky Mountain Taste and Smell Center, University of Colorado Denver Anschutz Medical Campus, Aurora, Colorado, United States of America.

ABSTRACT
On the basis of its primary circuit it has been postulated that the olfactory bulb (OB) is analogous to the retina in mammals. In retina, repeated exposure to the same visual stimulus results in a neural representation that remains relatively stable over time, even as the meaning of that stimulus to the animal changes. Stability of stimulus representation at early stages of processing allows for unbiased interpretation of incoming stimuli by higher order cortical centers. The alternative is that early stimulus representation is shaped by previously derived meaning, which could allow more efficient sampling of odor space providing a simplified yet biased interpretation of incoming stimuli. This study helps place the olfactory system on this continuum of subjective versus objective early sensory representation. Here we show that odor responses of the output cells of the OB, mitral cells, change transiently during a go-no-go odor discrimination task. The response changes occur in a manner that increases the ability of the circuit to convey information necessary to discriminate among closely related odors. Remarkably, a switch between which of the two odors is rewarded causes mitral cells to switch the polarity of their divergent responses. Taken together these results redefine the function of the OB as a transiently modifiable (active) filter, shaping early odor representations in behaviorally meaningful ways.

Show MeSH

Related in: MedlinePlus

Transient Firing Changes Observed during Learning(A) The top black plots display the behavior of the animal from which the unit data displayed in the lower plots was recorded. The behavior plot on the left corresponds to the two plots in the lower left and the upper right behavioral plot goes with the lower right rate change plot. The lower plots show unit firing rate change in response to odor A (red/rewarded) and odor AB (blue/ unrewarded) in each block of the behavior. The points represent the firing rate in spikes/0.15-s bins during odor exposure (0.5 to 2.5 s) minus the rate in spikes/0.15-s bin in the period before odor exposure (−1 to 0 s) (for details see Materials and Methods). Error bars denote mean +/− SEM of each point.(B) Bar graphs depicting the percent of total units that were responsive(red) and divergent (green) in the first, best, and last blocks. The data are from 189 single units (left) and 471 multiunits (right) recorded from eight different animals in 38 sessions.(C) The three pie charts illustrate the percent of total units (pooled single and multiunits) that were responsive (red) and divergent (green) in the first, best, and last blocks. The data are from 660 units recorded from eight different animals and 38 separate odor discriminations.
© Copyright Policy
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2573932&req=5

pbio-0060258-g004: Transient Firing Changes Observed during Learning(A) The top black plots display the behavior of the animal from which the unit data displayed in the lower plots was recorded. The behavior plot on the left corresponds to the two plots in the lower left and the upper right behavioral plot goes with the lower right rate change plot. The lower plots show unit firing rate change in response to odor A (red/rewarded) and odor AB (blue/ unrewarded) in each block of the behavior. The points represent the firing rate in spikes/0.15-s bins during odor exposure (0.5 to 2.5 s) minus the rate in spikes/0.15-s bin in the period before odor exposure (−1 to 0 s) (for details see Materials and Methods). Error bars denote mean +/− SEM of each point.(B) Bar graphs depicting the percent of total units that were responsive(red) and divergent (green) in the first, best, and last blocks. The data are from 189 single units (left) and 471 multiunits (right) recorded from eight different animals in 38 sessions.(C) The three pie charts illustrate the percent of total units (pooled single and multiunits) that were responsive (red) and divergent (green) in the first, best, and last blocks. The data are from 660 units recorded from eight different animals and 38 separate odor discriminations.

Mentions: In awake behaving animals there are MC responses to behavioral events such as poking the nose into the odor delivery chamber. As discussed in detail by Rinberg and coworkers [34], this fact makes it difficult to assign the changes in firing rate between pre- and peristimulus periods to odor responses unambiguously. Rinberg and coworkers propose detecting differences in firing rate between the rewarded and unrewarded odors in the peristimulus interval as a more robust method to determine odor responses. In this section we present comparisons of the difference in firing rate in a time window when the mouse is exposed to the odor as a robust measure of changes in firing rate caused by odor responses. The SMC whose firing is illustrated in the raster plots and peristimulus time histograms shown in Figure 3A and 3B appears to display a differential response to odors in blocks 5–7. The relationship of this cell's response divergence with the behavioral performance of the animal can be appreciated by comparing Figure 3A or 3B with Figure 3C where the percent of correct behavioral responses is plotted as a function of block number. Note that what we mean by response divergence is the difference in SMC firing rate during the peristimulus interval between rewarded odor trials and unrewarded odor trials computed on a block by block basis. It appears that the cell begins to diverge in its response to the unrewarded and rewarded odors at around block 5 while the animal does not begin performing at behavioral criterion (85% correct) until block 7. Indeed, when the changes in firing rates upon odor application (peristimulus minus prestimulus rates) are plotted as a function of block number for the reinforced and unreinforced odors (Figure 3D) the changes differ, not only across blocks, but also across stimuli (as shown by an ANOVA at p < 0.05). A post-hoc test shows that a statistically significant divergence in firing rate does in fact occur by block 5. Interestingly, the response is transient as evidenced by a lack of a statistical difference in a post hoc test between firing rates by the last block. Figure 4A shows other examples of the relationship of divergent firing between rewarded and unrewarded odor responses (all of these differed between stimuli when tested with ANOVA at p <0.05). The left plot of Figure 4A shows a unit that displayed differential firing from the beginning to the end of the session (very few units, two of 660, displayed differences throughout the session and this is shown here only for completeness). The center trace shows another unit from the same animal in which the unit develops a reduced firing rate response to the rewarded odor and no response—or perhaps a small excitatory response—to the unrewarded odor. The right plot in Figure 4A shows an example of a unit where the rewarded response is a stable decrease in the firing rate and the unrewarded response becomes a significantly larger decrease in firing rate than the rewarded response, developing into a divergent response.


Profound context-dependent plasticity of mitral cell responses in olfactory bulb.

Doucette W, Restrepo D - PLoS Biol. (2008)

Transient Firing Changes Observed during Learning(A) The top black plots display the behavior of the animal from which the unit data displayed in the lower plots was recorded. The behavior plot on the left corresponds to the two plots in the lower left and the upper right behavioral plot goes with the lower right rate change plot. The lower plots show unit firing rate change in response to odor A (red/rewarded) and odor AB (blue/ unrewarded) in each block of the behavior. The points represent the firing rate in spikes/0.15-s bins during odor exposure (0.5 to 2.5 s) minus the rate in spikes/0.15-s bin in the period before odor exposure (−1 to 0 s) (for details see Materials and Methods). Error bars denote mean +/− SEM of each point.(B) Bar graphs depicting the percent of total units that were responsive(red) and divergent (green) in the first, best, and last blocks. The data are from 189 single units (left) and 471 multiunits (right) recorded from eight different animals in 38 sessions.(C) The three pie charts illustrate the percent of total units (pooled single and multiunits) that were responsive (red) and divergent (green) in the first, best, and last blocks. The data are from 660 units recorded from eight different animals and 38 separate odor discriminations.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2573932&req=5

pbio-0060258-g004: Transient Firing Changes Observed during Learning(A) The top black plots display the behavior of the animal from which the unit data displayed in the lower plots was recorded. The behavior plot on the left corresponds to the two plots in the lower left and the upper right behavioral plot goes with the lower right rate change plot. The lower plots show unit firing rate change in response to odor A (red/rewarded) and odor AB (blue/ unrewarded) in each block of the behavior. The points represent the firing rate in spikes/0.15-s bins during odor exposure (0.5 to 2.5 s) minus the rate in spikes/0.15-s bin in the period before odor exposure (−1 to 0 s) (for details see Materials and Methods). Error bars denote mean +/− SEM of each point.(B) Bar graphs depicting the percent of total units that were responsive(red) and divergent (green) in the first, best, and last blocks. The data are from 189 single units (left) and 471 multiunits (right) recorded from eight different animals in 38 sessions.(C) The three pie charts illustrate the percent of total units (pooled single and multiunits) that were responsive (red) and divergent (green) in the first, best, and last blocks. The data are from 660 units recorded from eight different animals and 38 separate odor discriminations.
Mentions: In awake behaving animals there are MC responses to behavioral events such as poking the nose into the odor delivery chamber. As discussed in detail by Rinberg and coworkers [34], this fact makes it difficult to assign the changes in firing rate between pre- and peristimulus periods to odor responses unambiguously. Rinberg and coworkers propose detecting differences in firing rate between the rewarded and unrewarded odors in the peristimulus interval as a more robust method to determine odor responses. In this section we present comparisons of the difference in firing rate in a time window when the mouse is exposed to the odor as a robust measure of changes in firing rate caused by odor responses. The SMC whose firing is illustrated in the raster plots and peristimulus time histograms shown in Figure 3A and 3B appears to display a differential response to odors in blocks 5–7. The relationship of this cell's response divergence with the behavioral performance of the animal can be appreciated by comparing Figure 3A or 3B with Figure 3C where the percent of correct behavioral responses is plotted as a function of block number. Note that what we mean by response divergence is the difference in SMC firing rate during the peristimulus interval between rewarded odor trials and unrewarded odor trials computed on a block by block basis. It appears that the cell begins to diverge in its response to the unrewarded and rewarded odors at around block 5 while the animal does not begin performing at behavioral criterion (85% correct) until block 7. Indeed, when the changes in firing rates upon odor application (peristimulus minus prestimulus rates) are plotted as a function of block number for the reinforced and unreinforced odors (Figure 3D) the changes differ, not only across blocks, but also across stimuli (as shown by an ANOVA at p < 0.05). A post-hoc test shows that a statistically significant divergence in firing rate does in fact occur by block 5. Interestingly, the response is transient as evidenced by a lack of a statistical difference in a post hoc test between firing rates by the last block. Figure 4A shows other examples of the relationship of divergent firing between rewarded and unrewarded odor responses (all of these differed between stimuli when tested with ANOVA at p <0.05). The left plot of Figure 4A shows a unit that displayed differential firing from the beginning to the end of the session (very few units, two of 660, displayed differences throughout the session and this is shown here only for completeness). The center trace shows another unit from the same animal in which the unit develops a reduced firing rate response to the rewarded odor and no response—or perhaps a small excitatory response—to the unrewarded odor. The right plot in Figure 4A shows an example of a unit where the rewarded response is a stable decrease in the firing rate and the unrewarded response becomes a significantly larger decrease in firing rate than the rewarded response, developing into a divergent response.

Bottom Line: The response changes occur in a manner that increases the ability of the circuit to convey information necessary to discriminate among closely related odors.Remarkably, a switch between which of the two odors is rewarded causes mitral cells to switch the polarity of their divergent responses.Taken together these results redefine the function of the OB as a transiently modifiable (active) filter, shaping early odor representations in behaviorally meaningful ways.

View Article: PubMed Central - PubMed

Affiliation: Department of Cell and Developmental Biology, Neuroscience Program, Rocky Mountain Taste and Smell Center, University of Colorado Denver Anschutz Medical Campus, Aurora, Colorado, United States of America.

ABSTRACT
On the basis of its primary circuit it has been postulated that the olfactory bulb (OB) is analogous to the retina in mammals. In retina, repeated exposure to the same visual stimulus results in a neural representation that remains relatively stable over time, even as the meaning of that stimulus to the animal changes. Stability of stimulus representation at early stages of processing allows for unbiased interpretation of incoming stimuli by higher order cortical centers. The alternative is that early stimulus representation is shaped by previously derived meaning, which could allow more efficient sampling of odor space providing a simplified yet biased interpretation of incoming stimuli. This study helps place the olfactory system on this continuum of subjective versus objective early sensory representation. Here we show that odor responses of the output cells of the OB, mitral cells, change transiently during a go-no-go odor discrimination task. The response changes occur in a manner that increases the ability of the circuit to convey information necessary to discriminate among closely related odors. Remarkably, a switch between which of the two odors is rewarded causes mitral cells to switch the polarity of their divergent responses. Taken together these results redefine the function of the OB as a transiently modifiable (active) filter, shaping early odor representations in behaviorally meaningful ways.

Show MeSH
Related in: MedlinePlus