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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

Lick and Odor Responses Where the Animal Made Correct or Incorrect Behavioral Responses(A) Trial by trial rasters of lick behavior for the rewarded (odor A, left) and unrewarded (odor AB, right) odors. Red indicates periods of licking and blue indicates periods of no licking. Data for ten trials are shown for rewarded and unrewarded odors per block. Blocks are arranged from top to bottom. The green bar below the rasters indicates when the odor was delivered to the chamber. The yellow arrows point to trials where the animal made a mistake in the lick response.(B) Histograms of response magnitude normalized to the average correct rewarded (1) and unrewarded (0) firing rates during the peristimulus period sorted for the four different types of behavioral outcomes. The normalized response magnitude was calculated for each unit for all divergent units in 11 sessions in four animals (these were a subset of the 34 sessions in Figure 4 where the animal made six or more mistakes). Hits are trials where the animal licks sufficiently to obtain a water reward during a rewarded odor trial. Misses are trials in which the animal fails to lick sufficiently to receive reward on rewarded odor trials. Correct rejections (CR) are trials in which the animal refrains from licking during an unrewarded odor trial. False alarms (FA) are trials in which the animal responds by licking to an unrewarded odor as if it were a rewarded trial. The number of counts per bin represents the number of units displaying a response of a given normalized magnitude.
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pbio-0060258-g005: Lick and Odor Responses Where the Animal Made Correct or Incorrect Behavioral Responses(A) Trial by trial rasters of lick behavior for the rewarded (odor A, left) and unrewarded (odor AB, right) odors. Red indicates periods of licking and blue indicates periods of no licking. Data for ten trials are shown for rewarded and unrewarded odors per block. Blocks are arranged from top to bottom. The green bar below the rasters indicates when the odor was delivered to the chamber. The yellow arrows point to trials where the animal made a mistake in the lick response.(B) Histograms of response magnitude normalized to the average correct rewarded (1) and unrewarded (0) firing rates during the peristimulus period sorted for the four different types of behavioral outcomes. The normalized response magnitude was calculated for each unit for all divergent units in 11 sessions in four animals (these were a subset of the 34 sessions in Figure 4 where the animal made six or more mistakes). Hits are trials where the animal licks sufficiently to obtain a water reward during a rewarded odor trial. Misses are trials in which the animal fails to lick sufficiently to receive reward on rewarded odor trials. Correct rejections (CR) are trials in which the animal refrains from licking during an unrewarded odor trial. False alarms (FA) are trials in which the animal responds by licking to an unrewarded odor as if it were a rewarded trial. The number of counts per bin represents the number of units displaying a response of a given normalized magnitude.

Mentions: Figure 5A illustrates the licking responses for all trials in the experiment whose data were presented in Figure 3A. For each trial the bin was assigned a value of 1 (red) if there was a lick within a 0.15-s time bin or a value of zero (blue) if there were no licks in the time bin. The figure displays the licking behavior of the animal for rewarded odor trials (left) and unrewarded odor trials (right). Blue denotes periods when the mouse was not licking while red denotes licking and ten trials are shown for rewarded or unrewarded odors for each block. Blocks are displayed from top (first) to bottom (last). As shown, the animal learns to respond correctly by refraining from licking in the unrewarded odor trials. Rewarded odor trials in which the animal failed to lick sufficiently were called misses and successful trials were hits. The yellow arrow in the left panel shows a miss (an error that the animal made when it was supposed to lick during presentation of a rewarded trial) within a block where the majority of the responses were correct (hits). Unrewarded odor trials in which the animal licked as if it were the rewarded odor were called false alarms (FA) while trials in which the animal correctly refrained from licking were called correct rejections (CR). The yellow arrow head on the right panel in Figure 5A points to a false alarm in a block where the animal responded with correct rejections during the other unreinforced odor trials. For each unit/odor pair the average firing rate to the unrewarded and rewarded odor during the odor exposure period was normalized from zero to one respectively (Figure 5B). If the licking behavior or the expected outcome was driving the unit responses instead of the odor stimuli then the responses observed during error trials would be expected to resemble correct trials of the other odor. Figure 5B shows histograms compiling the normalized responses in 11 sessions in four animals (these were a subset of the 34 sessions in Figure 4 where the animal made six or more mistakes). The figure shows that for the unrewarded odor on trials when the animal treats it like a rewarded odor (FA) (licking with expectation of reward), the unit still responds with a firing rate that is not different from the correct rejection (CR) (p = 0.06, n = 30 units). Similarly, while error trials involving the rewarded odor differed between hits and misses (p = 0.001, n = 23), the normalized response magnitude for misses (Figure 5B) was much closer to one than to zero indicating that the observed unit responses are mainly odor responses and not a response to licking or some feedback representation from higher order areas of expected outcome.


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

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

Lick and Odor Responses Where the Animal Made Correct or Incorrect Behavioral Responses(A) Trial by trial rasters of lick behavior for the rewarded (odor A, left) and unrewarded (odor AB, right) odors. Red indicates periods of licking and blue indicates periods of no licking. Data for ten trials are shown for rewarded and unrewarded odors per block. Blocks are arranged from top to bottom. The green bar below the rasters indicates when the odor was delivered to the chamber. The yellow arrows point to trials where the animal made a mistake in the lick response.(B) Histograms of response magnitude normalized to the average correct rewarded (1) and unrewarded (0) firing rates during the peristimulus period sorted for the four different types of behavioral outcomes. The normalized response magnitude was calculated for each unit for all divergent units in 11 sessions in four animals (these were a subset of the 34 sessions in Figure 4 where the animal made six or more mistakes). Hits are trials where the animal licks sufficiently to obtain a water reward during a rewarded odor trial. Misses are trials in which the animal fails to lick sufficiently to receive reward on rewarded odor trials. Correct rejections (CR) are trials in which the animal refrains from licking during an unrewarded odor trial. False alarms (FA) are trials in which the animal responds by licking to an unrewarded odor as if it were a rewarded trial. The number of counts per bin represents the number of units displaying a response of a given normalized magnitude.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0060258-g005: Lick and Odor Responses Where the Animal Made Correct or Incorrect Behavioral Responses(A) Trial by trial rasters of lick behavior for the rewarded (odor A, left) and unrewarded (odor AB, right) odors. Red indicates periods of licking and blue indicates periods of no licking. Data for ten trials are shown for rewarded and unrewarded odors per block. Blocks are arranged from top to bottom. The green bar below the rasters indicates when the odor was delivered to the chamber. The yellow arrows point to trials where the animal made a mistake in the lick response.(B) Histograms of response magnitude normalized to the average correct rewarded (1) and unrewarded (0) firing rates during the peristimulus period sorted for the four different types of behavioral outcomes. The normalized response magnitude was calculated for each unit for all divergent units in 11 sessions in four animals (these were a subset of the 34 sessions in Figure 4 where the animal made six or more mistakes). Hits are trials where the animal licks sufficiently to obtain a water reward during a rewarded odor trial. Misses are trials in which the animal fails to lick sufficiently to receive reward on rewarded odor trials. Correct rejections (CR) are trials in which the animal refrains from licking during an unrewarded odor trial. False alarms (FA) are trials in which the animal responds by licking to an unrewarded odor as if it were a rewarded trial. The number of counts per bin represents the number of units displaying a response of a given normalized magnitude.
Mentions: Figure 5A illustrates the licking responses for all trials in the experiment whose data were presented in Figure 3A. For each trial the bin was assigned a value of 1 (red) if there was a lick within a 0.15-s time bin or a value of zero (blue) if there were no licks in the time bin. The figure displays the licking behavior of the animal for rewarded odor trials (left) and unrewarded odor trials (right). Blue denotes periods when the mouse was not licking while red denotes licking and ten trials are shown for rewarded or unrewarded odors for each block. Blocks are displayed from top (first) to bottom (last). As shown, the animal learns to respond correctly by refraining from licking in the unrewarded odor trials. Rewarded odor trials in which the animal failed to lick sufficiently were called misses and successful trials were hits. The yellow arrow in the left panel shows a miss (an error that the animal made when it was supposed to lick during presentation of a rewarded trial) within a block where the majority of the responses were correct (hits). Unrewarded odor trials in which the animal licked as if it were the rewarded odor were called false alarms (FA) while trials in which the animal correctly refrained from licking were called correct rejections (CR). The yellow arrow head on the right panel in Figure 5A points to a false alarm in a block where the animal responded with correct rejections during the other unreinforced odor trials. For each unit/odor pair the average firing rate to the unrewarded and rewarded odor during the odor exposure period was normalized from zero to one respectively (Figure 5B). If the licking behavior or the expected outcome was driving the unit responses instead of the odor stimuli then the responses observed during error trials would be expected to resemble correct trials of the other odor. Figure 5B shows histograms compiling the normalized responses in 11 sessions in four animals (these were a subset of the 34 sessions in Figure 4 where the animal made six or more mistakes). The figure shows that for the unrewarded odor on trials when the animal treats it like a rewarded odor (FA) (licking with expectation of reward), the unit still responds with a firing rate that is not different from the correct rejection (CR) (p = 0.06, n = 30 units). Similarly, while error trials involving the rewarded odor differed between hits and misses (p = 0.001, n = 23), the normalized response magnitude for misses (Figure 5B) was much closer to one than to zero indicating that the observed unit responses are mainly odor responses and not a response to licking or some feedback representation from higher order areas of expected outcome.

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