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Habituation of glomerular responses in the olfactory bulb following prolonged odor stimulation reflects reduced peripheral input.

Ogg MC, Bendahamane M, Fletcher ML - Front Mol Neurosci (2015)

Bottom Line: Currently, it is unclear if this decrease is a function of adaptation of peripheral olfactory sensory neuron (OSN) responses or reflects depression of bulb circuits.To test whether depression of OSN terminals contributed to this habituation, olfactory nerve layer (ON) stimulation was used to drive glomerular layer responses in the absence of peripheral odor activation of the OSNs.The difference in response between odor and electrical stimulation following odor habituation provides evidence that odor response reductions measured in the glomerular layer of the OB are most likely the result of OSN adaptation processes taking place in the periphery.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Neurobiology, University of Tennessee Health Science Center Memphis, TN, USA.

ABSTRACT
Following prolonged odor stimulation, output from olfactory bulb (OB) mitral/tufted (M/T) cells is decreased in response to subsequent olfactory stimulation. Currently, it is unclear if this decrease is a function of adaptation of peripheral olfactory sensory neuron (OSN) responses or reflects depression of bulb circuits. We used wide-field calcium imaging in anesthetized transgenic GCaMP2 mice to compare excitatory glomerular layer odor responses before and after a 30-s odor stimulation. Significant habituation of subsequent glomerular odor responses to both the same and structurally similar odorants was detected with our protocol. To test whether depression of OSN terminals contributed to this habituation, olfactory nerve layer (ON) stimulation was used to drive glomerular layer responses in the absence of peripheral odor activation of the OSNs. Following odor habituation, in contrast to odor-evoked glomerular responses, ON stimulation-evoked glomerular responses were not habituated. The difference in response between odor and electrical stimulation following odor habituation provides evidence that odor response reductions measured in the glomerular layer of the OB are most likely the result of OSN adaptation processes taking place in the periphery.

No MeSH data available.


Related in: MedlinePlus

Thirty seconds odor exposure decreases subsequent glomerular responses to a structurally similar odor. (A) Baseline glomerular responses to 2-heptanone (C7) and 2-hexanone (C6) in the same animal displayed in different color channels (C7, 0.5% s.v.: green; C6, 0.5% s.v.: red) at 10× magnification. (B) Overlay of the baseline glomerular responses to C7 and C6 shown in (A), highlighting glomeruli (yellow) that respond to both odors. White arrows indicate some examples of these shared glomeruli. (C) Pseudo-color glomerular responses to C7 and C6 before (Pre Hab) and after (Post C7 Hab) a 30-s exposure to C7. For both odors, glomerular responses are decreased from their baseline following the habituating odor exposure. (D) Mean normalized glomerular responses to both the habituated odor and the cross-habituated odor are reduced. Habituated responses are significantly lower than cross-habituated responses. (E) When C7 was used as the habituating odor, self- and cross-habituated responses were not significantly different. (F) When C6 was used as the habituating odor, self-habituated responses were significantly lower than cross-habituated responses. Error bars indicate SEM. *p < 0.05.
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Figure 3: Thirty seconds odor exposure decreases subsequent glomerular responses to a structurally similar odor. (A) Baseline glomerular responses to 2-heptanone (C7) and 2-hexanone (C6) in the same animal displayed in different color channels (C7, 0.5% s.v.: green; C6, 0.5% s.v.: red) at 10× magnification. (B) Overlay of the baseline glomerular responses to C7 and C6 shown in (A), highlighting glomeruli (yellow) that respond to both odors. White arrows indicate some examples of these shared glomeruli. (C) Pseudo-color glomerular responses to C7 and C6 before (Pre Hab) and after (Post C7 Hab) a 30-s exposure to C7. For both odors, glomerular responses are decreased from their baseline following the habituating odor exposure. (D) Mean normalized glomerular responses to both the habituated odor and the cross-habituated odor are reduced. Habituated responses are significantly lower than cross-habituated responses. (E) When C7 was used as the habituating odor, self- and cross-habituated responses were not significantly different. (F) When C6 was used as the habituating odor, self-habituated responses were significantly lower than cross-habituated responses. Error bars indicate SEM. *p < 0.05.

Mentions: We next evaluated whether prolonged exposure to an odor would affect the subsequent glomerular response to a structurally similar odor, an effect known as cross-habituation (Wilson, 2000). In five animals, pre-habituation baseline responses to 2-hexanone (C6) and 2-heptanone (C7) were established (Figure 3A). These odors differ by only a single carbon and share some activated glomeruli (Figure 3B). We assessed the effects of both self- and cross-habituation in shared glomeruli (Figure 3C). Pooling all habituation trials, regardless of habituating odor, shared glomeruli showed reduced mean normalized responses to both the habituated odor (59.1 ± 2.4% of baseline) and to the cross-habituated odor (66.9 ± 1.8% of baseline) with responses to the habituated odor significantly lower than those to the cross-habituated odor (paired t-test: t(61) = 2.53, p < 0.05, n = 62 glomeruli; Figure 3D). When the longer carbon chain odorant, C7, was used as the habituating odor, the cross-habituation (response to C6: 64.3 ± 2.4% of baseline) was not different from self-habituation (response to C7: 60.1 ± 3.1% of baseline; paired t-test: t(40) = 0.97, p = 0.33, n = 41 glomeruli; Figure 3E). However, when the shorter carbon chain odorant, C6, was used as the habituating odor, the cross-habituation (response to C7: 72.1 ± 2.7% of baseline) was significantly less than the self-habituation (response to C6: 57.3 ± 3.8% of baseline; paired t-test: t(20) = 4.92, p < 0.0001, n = 21 glomeruli; Figure 3F).


Habituation of glomerular responses in the olfactory bulb following prolonged odor stimulation reflects reduced peripheral input.

Ogg MC, Bendahamane M, Fletcher ML - Front Mol Neurosci (2015)

Thirty seconds odor exposure decreases subsequent glomerular responses to a structurally similar odor. (A) Baseline glomerular responses to 2-heptanone (C7) and 2-hexanone (C6) in the same animal displayed in different color channels (C7, 0.5% s.v.: green; C6, 0.5% s.v.: red) at 10× magnification. (B) Overlay of the baseline glomerular responses to C7 and C6 shown in (A), highlighting glomeruli (yellow) that respond to both odors. White arrows indicate some examples of these shared glomeruli. (C) Pseudo-color glomerular responses to C7 and C6 before (Pre Hab) and after (Post C7 Hab) a 30-s exposure to C7. For both odors, glomerular responses are decreased from their baseline following the habituating odor exposure. (D) Mean normalized glomerular responses to both the habituated odor and the cross-habituated odor are reduced. Habituated responses are significantly lower than cross-habituated responses. (E) When C7 was used as the habituating odor, self- and cross-habituated responses were not significantly different. (F) When C6 was used as the habituating odor, self-habituated responses were significantly lower than cross-habituated responses. Error bars indicate SEM. *p < 0.05.
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Figure 3: Thirty seconds odor exposure decreases subsequent glomerular responses to a structurally similar odor. (A) Baseline glomerular responses to 2-heptanone (C7) and 2-hexanone (C6) in the same animal displayed in different color channels (C7, 0.5% s.v.: green; C6, 0.5% s.v.: red) at 10× magnification. (B) Overlay of the baseline glomerular responses to C7 and C6 shown in (A), highlighting glomeruli (yellow) that respond to both odors. White arrows indicate some examples of these shared glomeruli. (C) Pseudo-color glomerular responses to C7 and C6 before (Pre Hab) and after (Post C7 Hab) a 30-s exposure to C7. For both odors, glomerular responses are decreased from their baseline following the habituating odor exposure. (D) Mean normalized glomerular responses to both the habituated odor and the cross-habituated odor are reduced. Habituated responses are significantly lower than cross-habituated responses. (E) When C7 was used as the habituating odor, self- and cross-habituated responses were not significantly different. (F) When C6 was used as the habituating odor, self-habituated responses were significantly lower than cross-habituated responses. Error bars indicate SEM. *p < 0.05.
Mentions: We next evaluated whether prolonged exposure to an odor would affect the subsequent glomerular response to a structurally similar odor, an effect known as cross-habituation (Wilson, 2000). In five animals, pre-habituation baseline responses to 2-hexanone (C6) and 2-heptanone (C7) were established (Figure 3A). These odors differ by only a single carbon and share some activated glomeruli (Figure 3B). We assessed the effects of both self- and cross-habituation in shared glomeruli (Figure 3C). Pooling all habituation trials, regardless of habituating odor, shared glomeruli showed reduced mean normalized responses to both the habituated odor (59.1 ± 2.4% of baseline) and to the cross-habituated odor (66.9 ± 1.8% of baseline) with responses to the habituated odor significantly lower than those to the cross-habituated odor (paired t-test: t(61) = 2.53, p < 0.05, n = 62 glomeruli; Figure 3D). When the longer carbon chain odorant, C7, was used as the habituating odor, the cross-habituation (response to C6: 64.3 ± 2.4% of baseline) was not different from self-habituation (response to C7: 60.1 ± 3.1% of baseline; paired t-test: t(40) = 0.97, p = 0.33, n = 41 glomeruli; Figure 3E). However, when the shorter carbon chain odorant, C6, was used as the habituating odor, the cross-habituation (response to C7: 72.1 ± 2.7% of baseline) was significantly less than the self-habituation (response to C6: 57.3 ± 3.8% of baseline; paired t-test: t(20) = 4.92, p < 0.0001, n = 21 glomeruli; Figure 3F).

Bottom Line: Currently, it is unclear if this decrease is a function of adaptation of peripheral olfactory sensory neuron (OSN) responses or reflects depression of bulb circuits.To test whether depression of OSN terminals contributed to this habituation, olfactory nerve layer (ON) stimulation was used to drive glomerular layer responses in the absence of peripheral odor activation of the OSNs.The difference in response between odor and electrical stimulation following odor habituation provides evidence that odor response reductions measured in the glomerular layer of the OB are most likely the result of OSN adaptation processes taking place in the periphery.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Neurobiology, University of Tennessee Health Science Center Memphis, TN, USA.

ABSTRACT
Following prolonged odor stimulation, output from olfactory bulb (OB) mitral/tufted (M/T) cells is decreased in response to subsequent olfactory stimulation. Currently, it is unclear if this decrease is a function of adaptation of peripheral olfactory sensory neuron (OSN) responses or reflects depression of bulb circuits. We used wide-field calcium imaging in anesthetized transgenic GCaMP2 mice to compare excitatory glomerular layer odor responses before and after a 30-s odor stimulation. Significant habituation of subsequent glomerular odor responses to both the same and structurally similar odorants was detected with our protocol. To test whether depression of OSN terminals contributed to this habituation, olfactory nerve layer (ON) stimulation was used to drive glomerular layer responses in the absence of peripheral odor activation of the OSNs. Following odor habituation, in contrast to odor-evoked glomerular responses, ON stimulation-evoked glomerular responses were not habituated. The difference in response between odor and electrical stimulation following odor habituation provides evidence that odor response reductions measured in the glomerular layer of the OB are most likely the result of OSN adaptation processes taking place in the periphery.

No MeSH data available.


Related in: MedlinePlus