Contextual Learning Induces Dendritic Spine Clustering in Retrosplenial Cortex
Adam
C.
Frank1, 2, 3, 4, 5,
Amos
Gdalyahu1, 2, 5,
Josh
Trachtenberg1, 2, 5 and
Alcino
J.
Silva1, 2, 3, 4, 5*
-
1
UCLA, Dept of Neurobiology, United States
-
2
UCLA, Integrative Center for Learning and Memory, United States
-
3
UCLA, Dept of Psychology, United States
-
4
UCLA, Dept of Psychiatry and Biobehavioral Sciences, United States
-
5
UCLA, Brain Research Institute, United States
Molecular and electrophysiological studies find convergent evidence suggesting that plasticity within a dendritic tree is not randomly dispersed, but rather clustered into functional groups. Further, results from in silico neuronal modeling show that clustered plasticity is able to increase storage capacity 45 times compared to dispersed plasticity. Recent in vivo work utilizing chronic 2-photon microscopy tested the clustering hypothesis and showed that repetitive motor learning is able to induce clustered addition of new dendritic spines on apical dendrites of L5 neurons in primary motor cortex; moreover, clustered spines were found to be more stable than non-clustered spines, suggesting a physiological role for spine clustering. To further test this hypothesis we used in vivo 2-photon imaging in Thy1-YFP-H mice to chronically examine dendritic spine dynamics in retrosplenial cortex (RSC) during spatial learning. RSC is a key component of an extended spatial learning and memory circuit that includes hippocampus and entorhinal cortex. Importantly, RSC is known from both lesion and immediate early gene studies to be critically involved in spatial learning and more specifically in contextual fear conditioning. We utilized a modified contextual fear conditioning protocol wherein animals received a mild foot shock each day for five days; this protocol induces gradual increases in context freezing over several days before the animals reach a behavioral plateau. We coupled behavioral training with four separate in vivo imaging sessions, two before training begins, one early in training, and a final session after training is complete. This allowed us to image spine dynamics before training as well as early in learning and after animals had reached behavioral asymptote. We find that this contextual learning protocol induces a statistically significant increase in the formation of clusters of new dendritic spines in trained animals when compared to home cage controls. Furthermore, most clustering occurs over the period where animals experience the largest increase in freezing behavior, suggesting that the clustered addition of spines may be subserving this learning process. Most importantly, the number of new clustered spines correlates with behavioral performance; specifically, animals with the highest proportion of new spines formed in clusters also have the highest context freezing, further supporting the hypothesis that clustered addition of spines is important for learning. In sum, these results support the hypothesis that spine clustering is a general mechanism for learning-related information storage in the brain and a mechanism specifically operating in the RSC.
Acknowledgements
This work was supported by an NIA grant to AJS and JTT (R37-AG013622) and a training grant (T32 MH 19384-15) to AF
Keywords:
retrosplenial cortex,
2-photon imaging,
Dendritic Spines,
contextual fear conditioning,
Spatial learning,
spine clustering,
clustered plasticity
Conference:
4th NAMASEN Training Workshop - Dendrites 2014, Heraklion, Greece, 1 Jul - 4 Jul, 2014.
Presentation Type:
Poster presentation
Topic:
morphological and functional characterizations
Citation:
Frank
AC,
Gdalyahu
A,
Trachtenberg
J and
Silva
AJ
(2014). Contextual Learning Induces Dendritic Spine Clustering in Retrosplenial Cortex.
Front. Syst. Neurosci.
Conference Abstract:
4th NAMASEN Training Workshop - Dendrites 2014.
doi: 10.3389/conf.fnsys.2014.05.00021
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Received:
11 Apr 2014;
Published Online:
12 Jun 2014.
*
Correspondence:
Dr. Alcino J Silva, UCLA, Dept of Neurobiology, Los Angeles, California, 90095, United States, silvaa@mednet.ucla.edu