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Distinct roles of basal forebrain cholinergic neurons in spatial and object recognition memory.

Okada K, Nishizawa K, Kobayashi T, Sakata S, Kobayashi K - Sci Rep (2015)

Bottom Line: Eliminating MS/vDB neurons impairs spatial but not object recognition memory in the reference and working memory tasks, whereas NBM elimination undermines only object recognition memory in the working memory task.These impairments are restored by treatment with acetylcholinesterase inhibitors, anti-dementia drugs for AD.Our results highlight that MS/vDB and NBM cholinergic neurons are not only implicated in recognition memory but also have essential roles in different types of recognition memory.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioural Sciences, Graduate School of Integrated Arts &Sciences, Hiroshima University, Higashi-Hiroshima 739-8521, Japan.

ABSTRACT
Recognition memory requires processing of various types of information such as objects and locations. Impairment in recognition memory is a prominent feature of amnesia and a symptom of Alzheimer's disease (AD). Basal forebrain cholinergic neurons contain two major groups, one localized in the medial septum (MS)/vertical diagonal band of Broca (vDB), and the other in the nucleus basalis magnocellularis (NBM). The roles of these cell groups in recognition memory have been debated, and it remains unclear how they contribute to it. We use a genetic cell targeting technique to selectively eliminate cholinergic cell groups and then test spatial and object recognition memory through different behavioural tasks. Eliminating MS/vDB neurons impairs spatial but not object recognition memory in the reference and working memory tasks, whereas NBM elimination undermines only object recognition memory in the working memory task. These impairments are restored by treatment with acetylcholinesterase inhibitors, anti-dementia drugs for AD. Our results highlight that MS/vDB and NBM cholinergic neurons are not only implicated in recognition memory but also have essential roles in different types of recognition memory.

No MeSH data available.


Related in: MedlinePlus

Targeting of the MS/vDB cholinergic neurons results in the impaired spatial reference memory.(a) Strategy for the serial object exploration task. A large circle indicates the circular open field with a striped board on the wall. Broken lines divide the open field into unit areas to measure locomotor activity. Mice individually explore the open field during seven successive sessions (S1–S7) that include the familiarization (S1), object exploration (S2–S4), displaced object exploration (S5/S6), and novel object exploration (S7) phases. Five different objects (A–E) were placed in the open field for S2–S4. Two objects (B,E) among these were displaced for S5/S6, and then one object (A) was exchanged by a novel object (F) in S7. (b,c) Mean number of contacts with objects during S2–S4. Tg and non-Tg mice were injected with IT solution or PBS into the MS/vDB (b) or NBM (c) and used for the task. Data are presented as mean ± s.e.m. n = 8 for each group. (d,e) Mean number of contacts with the non-displaced and displaced objects on a per-object basis in the spatial recognition test (S5). Mice injected with IT solution or PBS into the MS/vDB (d) or NBM (e) were used. Data are presented as mean ± s.e.m. n = 8 for each group. *P < 0.05 vs non-displaced object. NS, not significant. (f,g) Mean number of contacts with the non-displaced, displaced, and novel objects on a per-object basis in the object recognition test (S7). Mice injected with IT solution or PBS into the MS/vDB (f) or NBM (g) were used. Data are presented as mean ± s.e.m. n = 8 for each group. *P < 0.05 vs either non-displaced or displaced object.
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f2: Targeting of the MS/vDB cholinergic neurons results in the impaired spatial reference memory.(a) Strategy for the serial object exploration task. A large circle indicates the circular open field with a striped board on the wall. Broken lines divide the open field into unit areas to measure locomotor activity. Mice individually explore the open field during seven successive sessions (S1–S7) that include the familiarization (S1), object exploration (S2–S4), displaced object exploration (S5/S6), and novel object exploration (S7) phases. Five different objects (A–E) were placed in the open field for S2–S4. Two objects (B,E) among these were displaced for S5/S6, and then one object (A) was exchanged by a novel object (F) in S7. (b,c) Mean number of contacts with objects during S2–S4. Tg and non-Tg mice were injected with IT solution or PBS into the MS/vDB (b) or NBM (c) and used for the task. Data are presented as mean ± s.e.m. n = 8 for each group. (d,e) Mean number of contacts with the non-displaced and displaced objects on a per-object basis in the spatial recognition test (S5). Mice injected with IT solution or PBS into the MS/vDB (d) or NBM (e) were used. Data are presented as mean ± s.e.m. n = 8 for each group. *P < 0.05 vs non-displaced object. NS, not significant. (f,g) Mean number of contacts with the non-displaced, displaced, and novel objects on a per-object basis in the object recognition test (S7). Mice injected with IT solution or PBS into the MS/vDB (f) or NBM (g) were used. Data are presented as mean ± s.e.m. n = 8 for each group. *P < 0.05 vs either non-displaced or displaced object.

Mentions: To evaluate the impact of selective elimination of basal forebrain cholinergic neurons on spatial and object recognition memory in the reference memory task, we conducted a serial object exploration task3132. The task included seven successive sessions (S1–S7) consisting of the following four phases: (1) familiarization (S1), (2) object exploration (S2–S4), (3) displaced object exploration (S5/S6), and (4) novel object exploration (S7) (Fig. 2a). Mice were first familiarized in the open field during S1, and then explored the field, which contained five different objects, during S2–S4. Among these objects, two were displaced for S5/S6 and one was replaced with a novel object for S7. The number of contacts with objects was counted during each session except for S1. The number of contacts during S5 and S7 was used to assess spatial and object reference memory, respectively.


Distinct roles of basal forebrain cholinergic neurons in spatial and object recognition memory.

Okada K, Nishizawa K, Kobayashi T, Sakata S, Kobayashi K - Sci Rep (2015)

Targeting of the MS/vDB cholinergic neurons results in the impaired spatial reference memory.(a) Strategy for the serial object exploration task. A large circle indicates the circular open field with a striped board on the wall. Broken lines divide the open field into unit areas to measure locomotor activity. Mice individually explore the open field during seven successive sessions (S1–S7) that include the familiarization (S1), object exploration (S2–S4), displaced object exploration (S5/S6), and novel object exploration (S7) phases. Five different objects (A–E) were placed in the open field for S2–S4. Two objects (B,E) among these were displaced for S5/S6, and then one object (A) was exchanged by a novel object (F) in S7. (b,c) Mean number of contacts with objects during S2–S4. Tg and non-Tg mice were injected with IT solution or PBS into the MS/vDB (b) or NBM (c) and used for the task. Data are presented as mean ± s.e.m. n = 8 for each group. (d,e) Mean number of contacts with the non-displaced and displaced objects on a per-object basis in the spatial recognition test (S5). Mice injected with IT solution or PBS into the MS/vDB (d) or NBM (e) were used. Data are presented as mean ± s.e.m. n = 8 for each group. *P < 0.05 vs non-displaced object. NS, not significant. (f,g) Mean number of contacts with the non-displaced, displaced, and novel objects on a per-object basis in the object recognition test (S7). Mice injected with IT solution or PBS into the MS/vDB (f) or NBM (g) were used. Data are presented as mean ± s.e.m. n = 8 for each group. *P < 0.05 vs either non-displaced or displaced object.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4526880&req=5

f2: Targeting of the MS/vDB cholinergic neurons results in the impaired spatial reference memory.(a) Strategy for the serial object exploration task. A large circle indicates the circular open field with a striped board on the wall. Broken lines divide the open field into unit areas to measure locomotor activity. Mice individually explore the open field during seven successive sessions (S1–S7) that include the familiarization (S1), object exploration (S2–S4), displaced object exploration (S5/S6), and novel object exploration (S7) phases. Five different objects (A–E) were placed in the open field for S2–S4. Two objects (B,E) among these were displaced for S5/S6, and then one object (A) was exchanged by a novel object (F) in S7. (b,c) Mean number of contacts with objects during S2–S4. Tg and non-Tg mice were injected with IT solution or PBS into the MS/vDB (b) or NBM (c) and used for the task. Data are presented as mean ± s.e.m. n = 8 for each group. (d,e) Mean number of contacts with the non-displaced and displaced objects on a per-object basis in the spatial recognition test (S5). Mice injected with IT solution or PBS into the MS/vDB (d) or NBM (e) were used. Data are presented as mean ± s.e.m. n = 8 for each group. *P < 0.05 vs non-displaced object. NS, not significant. (f,g) Mean number of contacts with the non-displaced, displaced, and novel objects on a per-object basis in the object recognition test (S7). Mice injected with IT solution or PBS into the MS/vDB (f) or NBM (g) were used. Data are presented as mean ± s.e.m. n = 8 for each group. *P < 0.05 vs either non-displaced or displaced object.
Mentions: To evaluate the impact of selective elimination of basal forebrain cholinergic neurons on spatial and object recognition memory in the reference memory task, we conducted a serial object exploration task3132. The task included seven successive sessions (S1–S7) consisting of the following four phases: (1) familiarization (S1), (2) object exploration (S2–S4), (3) displaced object exploration (S5/S6), and (4) novel object exploration (S7) (Fig. 2a). Mice were first familiarized in the open field during S1, and then explored the field, which contained five different objects, during S2–S4. Among these objects, two were displaced for S5/S6 and one was replaced with a novel object for S7. The number of contacts with objects was counted during each session except for S1. The number of contacts during S5 and S7 was used to assess spatial and object reference memory, respectively.

Bottom Line: Eliminating MS/vDB neurons impairs spatial but not object recognition memory in the reference and working memory tasks, whereas NBM elimination undermines only object recognition memory in the working memory task.These impairments are restored by treatment with acetylcholinesterase inhibitors, anti-dementia drugs for AD.Our results highlight that MS/vDB and NBM cholinergic neurons are not only implicated in recognition memory but also have essential roles in different types of recognition memory.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioural Sciences, Graduate School of Integrated Arts &Sciences, Hiroshima University, Higashi-Hiroshima 739-8521, Japan.

ABSTRACT
Recognition memory requires processing of various types of information such as objects and locations. Impairment in recognition memory is a prominent feature of amnesia and a symptom of Alzheimer's disease (AD). Basal forebrain cholinergic neurons contain two major groups, one localized in the medial septum (MS)/vertical diagonal band of Broca (vDB), and the other in the nucleus basalis magnocellularis (NBM). The roles of these cell groups in recognition memory have been debated, and it remains unclear how they contribute to it. We use a genetic cell targeting technique to selectively eliminate cholinergic cell groups and then test spatial and object recognition memory through different behavioural tasks. Eliminating MS/vDB neurons impairs spatial but not object recognition memory in the reference and working memory tasks, whereas NBM elimination undermines only object recognition memory in the working memory task. These impairments are restored by treatment with acetylcholinesterase inhibitors, anti-dementia drugs for AD. Our results highlight that MS/vDB and NBM cholinergic neurons are not only implicated in recognition memory but also have essential roles in different types of recognition memory.

No MeSH data available.


Related in: MedlinePlus