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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

Divergence in Single Unit Responses during Learning in the Odor Discrimination Task(A) Raster plot of single unit spike times organized per block for the ten rewarded trials (A, left column) and ten unrewarded trials (AB, right column). Timing and duration of odor exposure is indicated on the x-axis by the red bar.(B) PSTH of the data shown in (A). Red lines on either side of the histogram indicate +/− standard error of the mean (SEM). The bin size in the PSTH is 0.15 s. This means that the firing rate in Hz is the value in the y-axis × (1/0.15).(C) Behavioral performance—percent correct as a function of block number—for the animal from whom the cell in (A) and (B) was recorded.(D) A plot of the firing-rate increase above background to odor A (red) and odor AB (blue) in each block of the behavior. The points represent the firing rate in spikes/0.15-s bin during odor exposure (0.5 to 2.5 s) minus the rate in spikes/0.15-s bin in the period immediately before odor exposure (−1 to 0 s). Error bars denote the mean +/− SEM of each point (ten trials per point).(E) The lower right hand pie chart shows what percent of the responses were inhibitory (gray), excitatory (yellow), or mixed (blue). A mixed response was defined as a response to either odor A or AB that had both an excitatory and inhibitory component or a response that was excitatory to one odor and inhibitory to the other odor stimulus.
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pbio-0060258-g003: Divergence in Single Unit Responses during Learning in the Odor Discrimination Task(A) Raster plot of single unit spike times organized per block for the ten rewarded trials (A, left column) and ten unrewarded trials (AB, right column). Timing and duration of odor exposure is indicated on the x-axis by the red bar.(B) PSTH of the data shown in (A). Red lines on either side of the histogram indicate +/− standard error of the mean (SEM). The bin size in the PSTH is 0.15 s. This means that the firing rate in Hz is the value in the y-axis × (1/0.15).(C) Behavioral performance—percent correct as a function of block number—for the animal from whom the cell in (A) and (B) was recorded.(D) A plot of the firing-rate increase above background to odor A (red) and odor AB (blue) in each block of the behavior. The points represent the firing rate in spikes/0.15-s bin during odor exposure (0.5 to 2.5 s) minus the rate in spikes/0.15-s bin in the period immediately before odor exposure (−1 to 0 s). Error bars denote the mean +/− SEM of each point (ten trials per point).(E) The lower right hand pie chart shows what percent of the responses were inhibitory (gray), excitatory (yellow), or mixed (blue). A mixed response was defined as a response to either odor A or AB that had both an excitatory and inhibitory component or a response that was excitatory to one odor and inhibitory to the other odor stimulus.

Mentions: Figure 3A displays a raster plot and Figure 3B shows the corresponding peristimulus histogram (PSTH) depicting the firing of a single unit during an olfactory discrimination task. The left panel shows activity during the rewarded odor trials (odor A) and the right panel shows activity of the SMC for the unrewarded odor (odor AB) trials. Each block of 20 trials (ten rewarded and ten unrewarded) is represented by the set of ten rows in the right panel (unrewarded) and the corresponding set of ten rows in the left panel (rewarded). The nine blocks that composed the learning session are displayed from top to bottom. Figure 3A illustrates how the odor response of one SMC evolves as the animal learns to discriminate between the two odors, developing what appears to be an excitatory response to the rewarded odor and no response to the unrewarded odor. In order to determine whether the firing rate during odor exposure (peristimulus interval) differed significantly from the firing rate before odor exposure (prestimulus interval), we used a t-test with correction for multiple comparisons to compare the difference between the firing rate in the prestimulus interval (−1 to 0 s) to the firing rate in small windows (0.75 s) scanned across the peristimulus interval (0.5 to 3.125 s) by 0.325-s steps (see Materials and Methods). The p-values of this test for significant responses for the SMC shown in Figure 3A are displayed in Table 1. The rewarded odor induced significant changes in firing rate in blocks 5, 6, and 7 and the unrewarded odor elicited a significant change in block 3.


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

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

Divergence in Single Unit Responses during Learning in the Odor Discrimination Task(A) Raster plot of single unit spike times organized per block for the ten rewarded trials (A, left column) and ten unrewarded trials (AB, right column). Timing and duration of odor exposure is indicated on the x-axis by the red bar.(B) PSTH of the data shown in (A). Red lines on either side of the histogram indicate +/− standard error of the mean (SEM). The bin size in the PSTH is 0.15 s. This means that the firing rate in Hz is the value in the y-axis × (1/0.15).(C) Behavioral performance—percent correct as a function of block number—for the animal from whom the cell in (A) and (B) was recorded.(D) A plot of the firing-rate increase above background to odor A (red) and odor AB (blue) in each block of the behavior. The points represent the firing rate in spikes/0.15-s bin during odor exposure (0.5 to 2.5 s) minus the rate in spikes/0.15-s bin in the period immediately before odor exposure (−1 to 0 s). Error bars denote the mean +/− SEM of each point (ten trials per point).(E) The lower right hand pie chart shows what percent of the responses were inhibitory (gray), excitatory (yellow), or mixed (blue). A mixed response was defined as a response to either odor A or AB that had both an excitatory and inhibitory component or a response that was excitatory to one odor and inhibitory to the other odor stimulus.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0060258-g003: Divergence in Single Unit Responses during Learning in the Odor Discrimination Task(A) Raster plot of single unit spike times organized per block for the ten rewarded trials (A, left column) and ten unrewarded trials (AB, right column). Timing and duration of odor exposure is indicated on the x-axis by the red bar.(B) PSTH of the data shown in (A). Red lines on either side of the histogram indicate +/− standard error of the mean (SEM). The bin size in the PSTH is 0.15 s. This means that the firing rate in Hz is the value in the y-axis × (1/0.15).(C) Behavioral performance—percent correct as a function of block number—for the animal from whom the cell in (A) and (B) was recorded.(D) A plot of the firing-rate increase above background to odor A (red) and odor AB (blue) in each block of the behavior. The points represent the firing rate in spikes/0.15-s bin during odor exposure (0.5 to 2.5 s) minus the rate in spikes/0.15-s bin in the period immediately before odor exposure (−1 to 0 s). Error bars denote the mean +/− SEM of each point (ten trials per point).(E) The lower right hand pie chart shows what percent of the responses were inhibitory (gray), excitatory (yellow), or mixed (blue). A mixed response was defined as a response to either odor A or AB that had both an excitatory and inhibitory component or a response that was excitatory to one odor and inhibitory to the other odor stimulus.
Mentions: Figure 3A displays a raster plot and Figure 3B shows the corresponding peristimulus histogram (PSTH) depicting the firing of a single unit during an olfactory discrimination task. The left panel shows activity during the rewarded odor trials (odor A) and the right panel shows activity of the SMC for the unrewarded odor (odor AB) trials. Each block of 20 trials (ten rewarded and ten unrewarded) is represented by the set of ten rows in the right panel (unrewarded) and the corresponding set of ten rows in the left panel (rewarded). The nine blocks that composed the learning session are displayed from top to bottom. Figure 3A illustrates how the odor response of one SMC evolves as the animal learns to discriminate between the two odors, developing what appears to be an excitatory response to the rewarded odor and no response to the unrewarded odor. In order to determine whether the firing rate during odor exposure (peristimulus interval) differed significantly from the firing rate before odor exposure (prestimulus interval), we used a t-test with correction for multiple comparisons to compare the difference between the firing rate in the prestimulus interval (−1 to 0 s) to the firing rate in small windows (0.75 s) scanned across the peristimulus interval (0.5 to 3.125 s) by 0.325-s steps (see Materials and Methods). The p-values of this test for significant responses for the SMC shown in Figure 3A are displayed in Table 1. The rewarded odor induced significant changes in firing rate in blocks 5, 6, and 7 and the unrewarded odor elicited a significant change in block 3.

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