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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.

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Related in: MedlinePlus

Changes in MC Odor Responses during Reversal(A) PSTH for a multiunit response to odors A and AB during an initial discrimination (day 1) whose behavioral performance curve (percent correct responses versus block number) is displayed in (D) (left). This unit never develops a significant response to A but develops a significant inhibitory response to AB.(B) The same multiunit responding the next day (day 2) in the performance of a reversal task in which the reward associations of odor A and AB had been reversed (the behavioral curve is displayed in the right side of [D]). The unit developed a significant inhibitory response to odor A (now unrewarded) and a significant excitatory response to odor AB (now rewarded). The red bar under the time axis denotes the interval when the mouse was exposed to the odor.(C) Odor-elicited firing-rate changes observed during day 1 (left) and during reversal in day 2 (right). The two plots show unit firing-rate change in response to odor A (red) and odor AB (blue) in each block of the session. 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 (n = 10 rewarded and 10 unrewarded odors per block). An ANOVA indicated that in both day 1 and day 2 the responses to odor A differed from responses to odor AB (p < 0.05).(D) Percent correct responses for the behavior in the first day task (left) and the second day reversal (right).(E) Summary of all reversal experiments consisting of 358 units from eight animals and 24 different reversal sessions.(F) Pie illustrating what happens to units that are divergent in either the initial discrimination or the reversal. “No Divergent Pair” indicates that the unit only had statistically significant divergence in one of the two complementary tasks. “Valence Switch” means that the odor evoked firing rates switched from A>AB to A<AB or vice versa from the initial discrimination to the reversal. “Valence Same” indicates that the odor evoked firing rates maintain their relationship A>AB to A>AB or vice versa from the initial discrimination to the reversal.
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pbio-0060258-g006: Changes in MC Odor Responses during Reversal(A) PSTH for a multiunit response to odors A and AB during an initial discrimination (day 1) whose behavioral performance curve (percent correct responses versus block number) is displayed in (D) (left). This unit never develops a significant response to A but develops a significant inhibitory response to AB.(B) The same multiunit responding the next day (day 2) in the performance of a reversal task in which the reward associations of odor A and AB had been reversed (the behavioral curve is displayed in the right side of [D]). The unit developed a significant inhibitory response to odor A (now unrewarded) and a significant excitatory response to odor AB (now rewarded). The red bar under the time axis denotes the interval when the mouse was exposed to the odor.(C) Odor-elicited firing-rate changes observed during day 1 (left) and during reversal in day 2 (right). The two plots show unit firing-rate change in response to odor A (red) and odor AB (blue) in each block of the session. 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 (n = 10 rewarded and 10 unrewarded odors per block). An ANOVA indicated that in both day 1 and day 2 the responses to odor A differed from responses to odor AB (p < 0.05).(D) Percent correct responses for the behavior in the first day task (left) and the second day reversal (right).(E) Summary of all reversal experiments consisting of 358 units from eight animals and 24 different reversal sessions.(F) Pie illustrating what happens to units that are divergent in either the initial discrimination or the reversal. “No Divergent Pair” indicates that the unit only had statistically significant divergence in one of the two complementary tasks. “Valence Switch” means that the odor evoked firing rates switched from A>AB to A<AB or vice versa from the initial discrimination to the reversal. “Valence Same” indicates that the odor evoked firing rates maintain their relationship A>AB to A>AB or vice versa from the initial discrimination to the reversal.

Mentions: Figure 6A shows the PSTHs for rewarded (odor A, left) and unrewarded (odor AB, right) odors for a multiunit from an animal that has not previously been shown. The left panel in Figure 6C shows the corresponding change in firing rate elicited by the reinforced (red, odor A) and unreinforced (blue, odor AB) odors as a function of the number of blocks, and the left learning curve in Figure 6D shows the corresponding behavioral performance curve. There is no significant change across blocks in response to the rewarded odor (A) but there is development of a reduced firing rate response to the unrewarded odor (AB). Figure 6B displays neural activity recorded from the same electrode as in Figure 6A the following day during a reversal of the reward to odors A and AB, and the corresponding plot in Figure 6C (right) shows the change in firing rate elicited by the odor A (red) that is now unreinforced and odor AB (blue) that is now reinforced as a function of the number of blocks. The plot on the right in Figure 6D shows the corresponding progress through the learning curve as the animal learns the new associations of the odors (A, unrewarded and AB, rewarded; the left plot is the learning curve for the first day A, rewarded and AB, unrewarded). What is interesting is that as the animal learns to make these new associations the unit's response changes polarity. Now in response to the same odor (AB) that resulted in a significant reduced firing rate response on day 1, cells recorded from the same electrode on day 2 developed a significant excitatory response (compare blue curves in the two panels in Figure 6C). It is also important to note that the reduced firing rate response to odor AB gained during the initial discrimination is not present at the beginning of the reversal the following day. This switch was observed for the majority of units that developed divergence for odor responsiveness in the first day and was subsequently tested for reversal the next day (compare the green slice in the first block in Figure 6E with the green slice in the best and last blocks in Figure 4C, Chi2 < 0.05). This further illustrates that the observed changes occurring during discriminations are transient, not persisting to the following day.


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

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

Changes in MC Odor Responses during Reversal(A) PSTH for a multiunit response to odors A and AB during an initial discrimination (day 1) whose behavioral performance curve (percent correct responses versus block number) is displayed in (D) (left). This unit never develops a significant response to A but develops a significant inhibitory response to AB.(B) The same multiunit responding the next day (day 2) in the performance of a reversal task in which the reward associations of odor A and AB had been reversed (the behavioral curve is displayed in the right side of [D]). The unit developed a significant inhibitory response to odor A (now unrewarded) and a significant excitatory response to odor AB (now rewarded). The red bar under the time axis denotes the interval when the mouse was exposed to the odor.(C) Odor-elicited firing-rate changes observed during day 1 (left) and during reversal in day 2 (right). The two plots show unit firing-rate change in response to odor A (red) and odor AB (blue) in each block of the session. 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 (n = 10 rewarded and 10 unrewarded odors per block). An ANOVA indicated that in both day 1 and day 2 the responses to odor A differed from responses to odor AB (p < 0.05).(D) Percent correct responses for the behavior in the first day task (left) and the second day reversal (right).(E) Summary of all reversal experiments consisting of 358 units from eight animals and 24 different reversal sessions.(F) Pie illustrating what happens to units that are divergent in either the initial discrimination or the reversal. “No Divergent Pair” indicates that the unit only had statistically significant divergence in one of the two complementary tasks. “Valence Switch” means that the odor evoked firing rates switched from A>AB to A<AB or vice versa from the initial discrimination to the reversal. “Valence Same” indicates that the odor evoked firing rates maintain their relationship A>AB to A>AB or vice versa from the initial discrimination to the reversal.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0060258-g006: Changes in MC Odor Responses during Reversal(A) PSTH for a multiunit response to odors A and AB during an initial discrimination (day 1) whose behavioral performance curve (percent correct responses versus block number) is displayed in (D) (left). This unit never develops a significant response to A but develops a significant inhibitory response to AB.(B) The same multiunit responding the next day (day 2) in the performance of a reversal task in which the reward associations of odor A and AB had been reversed (the behavioral curve is displayed in the right side of [D]). The unit developed a significant inhibitory response to odor A (now unrewarded) and a significant excitatory response to odor AB (now rewarded). The red bar under the time axis denotes the interval when the mouse was exposed to the odor.(C) Odor-elicited firing-rate changes observed during day 1 (left) and during reversal in day 2 (right). The two plots show unit firing-rate change in response to odor A (red) and odor AB (blue) in each block of the session. 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 (n = 10 rewarded and 10 unrewarded odors per block). An ANOVA indicated that in both day 1 and day 2 the responses to odor A differed from responses to odor AB (p < 0.05).(D) Percent correct responses for the behavior in the first day task (left) and the second day reversal (right).(E) Summary of all reversal experiments consisting of 358 units from eight animals and 24 different reversal sessions.(F) Pie illustrating what happens to units that are divergent in either the initial discrimination or the reversal. “No Divergent Pair” indicates that the unit only had statistically significant divergence in one of the two complementary tasks. “Valence Switch” means that the odor evoked firing rates switched from A>AB to A<AB or vice versa from the initial discrimination to the reversal. “Valence Same” indicates that the odor evoked firing rates maintain their relationship A>AB to A>AB or vice versa from the initial discrimination to the reversal.
Mentions: Figure 6A shows the PSTHs for rewarded (odor A, left) and unrewarded (odor AB, right) odors for a multiunit from an animal that has not previously been shown. The left panel in Figure 6C shows the corresponding change in firing rate elicited by the reinforced (red, odor A) and unreinforced (blue, odor AB) odors as a function of the number of blocks, and the left learning curve in Figure 6D shows the corresponding behavioral performance curve. There is no significant change across blocks in response to the rewarded odor (A) but there is development of a reduced firing rate response to the unrewarded odor (AB). Figure 6B displays neural activity recorded from the same electrode as in Figure 6A the following day during a reversal of the reward to odors A and AB, and the corresponding plot in Figure 6C (right) shows the change in firing rate elicited by the odor A (red) that is now unreinforced and odor AB (blue) that is now reinforced as a function of the number of blocks. The plot on the right in Figure 6D shows the corresponding progress through the learning curve as the animal learns the new associations of the odors (A, unrewarded and AB, rewarded; the left plot is the learning curve for the first day A, rewarded and AB, unrewarded). What is interesting is that as the animal learns to make these new associations the unit's response changes polarity. Now in response to the same odor (AB) that resulted in a significant reduced firing rate response on day 1, cells recorded from the same electrode on day 2 developed a significant excitatory response (compare blue curves in the two panels in Figure 6C). It is also important to note that the reduced firing rate response to odor AB gained during the initial discrimination is not present at the beginning of the reversal the following day. This switch was observed for the majority of units that developed divergence for odor responsiveness in the first day and was subsequently tested for reversal the next day (compare the green slice in the first block in Figure 6E with the green slice in the best and last blocks in Figure 4C, Chi2 < 0.05). This further illustrates that the observed changes occurring during discriminations are transient, not persisting to the following day.

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