Temporary inactivation of the supramammillary area impairs spatial working memory and spatial reference memory retrieval

Aranda, Lourdes; Begega, Azucena; Sánchez-López, Jorge; Aguirre, J.A.; Árias, Jorge L.; Santín, Luis J.

doi:10.1016/j.physbeh.2008.01.024

Cited by 28 publications

(17 citation statements)

References 22 publications

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“…Many previous studies have demonstrated a role for SuM in HPC-related learning (Pan and McNaughton, 1997;Shahidi et al, 2004;Aranda et al, 2008). A positive correlation between HPC theta frequency and a SuM to HPC direction of theta propagation was also reported previously with anesthetized animals (Kocsis and Kaminski, 2006).…”

Section: Discussionsupporting

confidence: 77%

Minimal driving of hippocampal theta by the supramammillary nucleus during water maze learning

2011

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Previous studies have shown only modest effects of supramammillary nucleus (SuM) dysfunction on theta frequency and learning in the water maze (WM), with larger effects in other tasks. However, theta recorded from SuM, and used to trigger the production of theta-like oscillations in the hippocampus, produced reversal of the deficit in WM learning produced by theta blocking. We explored this apparent inconsistency by analyzing the relationship between SuM and hippocampal theta in the control group of this theta-blocking experiment using coherence, phase analysis, and the directed transfer function. We found little evidence of an influence of SuM on the hippocampus in the bulk of WM learning-with some possibility of SuM becoming involved briefly later in learning. A learning-related increase in coherence was observed in conjunction with gradual phase reorganization of hippocampal theta in relation to SuM theta. This change in phase dynamics between the two structures was also correlated with a relative increase of the estimated direction of theta propagation from the SuM to the hippocampus. These results are consistent with the previous weak effects of SuM lesions and suggest that the use of SuM as a source to trigger hippocampal theta and recover function is likely to be due to coherence between SuM and some other structure that normally controls hippocampal theta during WM learning.

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Section: Discussionsupporting

confidence: 77%

Minimal driving of hippocampal theta by the supramammillary nucleus during water maze learning

2011

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“…Moreover, reversible inactivation of the SUM with lidocaine impaired consolidation of the reference memory version of the Morris water maze (Shahidi et al, 2004). Nevertheless, Aranda et al (2008) showed that SUM lesions impair the capacity of rats to solve spatial working but not reference memory tasks in an open field. Based on the heterogeneous set of behavioural data published, Pan and McNaughton (2004) suggested that it is a key part of a network that recursively transforms information to achieve integration of cognitive and emotional aspects of goal-directed behaviour.…”

Section: Discussionmentioning

confidence: 98%

“…Specifically, evidence was found of higher CO activity in SUM and MMN in spatial learning associated both with allocentric and egocentric strategies, compared to the control group. Previous studies of our laboratory using lesion approach, c-fos expression and CO activity with different procedures have revealed the behavioural role of the mammillary bodies in spatial alternation, spatial working memory and spatial reference memory (Santı´n et al, 1999(Santı´n et al, , 2003Aranda et al, 2008;Begega et al, 2010;Conejo et al, 2010).…”

Section: Discussionmentioning

confidence: 99%

Similarities and differences between the brain networks underlying allocentric and egocentric spatial learning in rat revealed by cytochrome oxidase histochemistry

et al. 2012

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“…Shahidi et al (2004b) subsequently demonstrated that suppressing SUM altered performance on spatial reference memory (RM) and working memory (WM) tasks on the water maze; that is, disrupting consolidation on the RM task and both consolidation and retrieval on the WM task. Supporting this, electrolytic lesions (Aranda et al, 2006) or the reversible inactivation of SUM (Aranda et al, 2008) impaired spatial WM on a delayed-matching-to-position task. It was further reported (Aranda et al, 2006) that SUM lesions produced anxiolytic effects on an elevated T-maze.…”

Section: Sum: Role In Learning and Memorymentioning

confidence: 84%

“…As might be expected by relatively widespread SUM projections to the limbic forebrain, the SUM has been associated with various functions including stress, anxiety, response to novelty, reward processes, and learning/memory (Aranda et al, 2006, 2008; Choi et al, 2012; Ikemoto, 2005; Ikemoto and Bonci, 2014; Ito et al, 2009; Shahidi et al, 2004a,b). Perhaps owing to the strong SUM projections to the septum and the hippocampus, disruptions of SUM have been shown to severely impair learning/memory over a range of tasks.…”

Section: Sum: Role In Learning and Memorymentioning

confidence: 87%

Major diencephalic inputs to the hippocampus

Vertes

2015

Progress in Brain Research

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The hippocampus receives two major external inputs from the diencephalon, that is, from the supramammillary nucleus (SUM) and nucleus reuniens (RE) of the midline thalamus. These two afferents systems project to separate, nonoverlapping, regions of the hippocampus. Specifically, the SUM distributes to the dentate gyrus (DG) and to CA2 of the dorsal and ventral hippocampus, whereas RE projects to CA1 of the dorsal and ventral hippocampus and to the subiculum. SUM and RE fibers to the hippocampus participate in common as well as in separate functions. Both systems would appear to amplify signals from other sources to their respective hippocampal targets. SUM amplifies signals from the entorhinal cortex (EC) to DG, whereas RE may amplify them from CA3 (and EC) to CA1 of the hippocampus. This “amplification” may serve to promote the transfer, encoding, and possibly storage of information from EC to DG and from CA3 and EC to CA1. Regarding their unique actions on the hippocampus, the SUM is a vital part of an ascending brainstem to hippocampal system generating the theta rhythm of the hippocampus, whereas RE importantly routes information from the medial prefrontal cortex to the hippocampus to thereby mediate functions involving both structures. In summary, although, to date, SUM and RE afferents to the hippocampus have not been extensively explored, the SUM and RE exert a profound influence on the hippocampus in processes of learning and memory.

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Temporary inactivation of the supramammillary area impairs spatial working memory and spatial reference memory retrieval

Cited by 28 publications

References 22 publications

Minimal driving of hippocampal theta by the supramammillary nucleus during water maze learning

Minimal driving of hippocampal theta by the supramammillary nucleus during water maze learning

Similarities and differences between the brain networks underlying allocentric and egocentric spatial learning in rat revealed by cytochrome oxidase histochemistry

Major diencephalic inputs to the hippocampus

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