Input clustering and the microscale structure of local circuits

DeBello, William M.; McBride, Thomas J.; Nichols, Grant S.; Pannoni, Katy E.; Sanculi, Daniel; Totten, Douglas

doi:10.3389/fncir.2014.00112

Cited by 37 publications

(40 citation statements)

References 139 publications

(148 reference statements)

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“…The size and location of these dendritic compartments are not fixed and can dynamically change according to the activation and input pattern Behabadi et al, 2012;Jadi et al, 2012;Major et al, 2013). Recent studies support the notion of anatomical and functional clustering of synapses to dendritic compartments both during development and learning (Fu et al, 2012;Takahashi et al, 2012;DeBello et al, 2014;Druckmann et al, 2014;Cichon and Gan, 2015), in line with the possibility that dendritic branchlets may serve as key plasticity and storage elements during learning (Mel, 1992;Poirazi and Mel, 2001;Chklovskii et al, 2004).…”

Section: Compartmentalized Plasticity Mechanismsmentioning

confidence: 83%

A Novel Form of Local Plasticity in Tuft Dendrites of Neocortical Somatosensory Layer 5 Pyramidal Neurons

Sandler

Shulman

Schiller

2016

Neuron

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Tuft dendrites of layer 5 pyramidal neurons form a separate biophysical and processing compartment. Presently, little is known about plasticity mechanisms in this isolated compartment. Here, we describe a novel form of plasticity in which unpaired low-frequency (0.1 Hz) stimulation of tuft inputs resulted in prolonged transient (86.3 ± 7.3 min) potentiation of EPSPs (286.1% ± 30.5%) and enhanced local excitability that enabled more-efficient back-propagation of axo-somatic action potentials and dendritic calcium spikes selectively into the activated dendritic segments. This plasticity was exclusive to tuft dendrites and did not occur in basal dendrites. Induction of this plasticity depended on activation of Kv4.2 potassium and NMDAR channels, internalization of membrane proteins, and insertion of AMPAR. This unique form of tuft plasticity increases proximal-distal electrical coupling of activated tuft dendrites and opens a prolonged time window for binding and storing feedforward and feedback information in a branch-specific manner.

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Section: Compartmentalized Plasticity Mechanismsmentioning

confidence: 83%

A Novel Form of Local Plasticity in Tuft Dendrites of Neocortical Somatosensory Layer 5 Pyramidal Neurons

Sandler

Shulman

Schiller

2016

Neuron

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“…Overall, the large number of studies providing experimental evidence for both anatomical and functional synaptic clustering (some examples are shown in Figure 2) suggests that clustering may be a common pattern of organization conserved across different brain areas and species (DeBello et al, 2014). …”

Section: Dendritic Branches As Key Computational Elementsmentioning

confidence: 99%

Synaptic clustering within dendrites: An emerging theory of memory formation

Kastellakis

Cai²,

Mednick

et al. 2015

Progress in Neurobiology

165

139

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It is generally accepted that complex memories are stored in distributed representations throughout the brain, however the mechanisms underlying these representations are not understood. Here, we review recent findings regarding the subcellular mechanisms implicated in memory formation, which provide evidence for a dendrite-centered theory of memory. Plasticity-related phenomena which affect synaptic properties, such as synaptic tagging and capture, synaptic clustering, branch strength potentiation and spinogenesis provide the foundation for a model of memory storage that relies heavily on processes operating at the dendrite level. The emerging picture suggests that clusters of functionally related synapses may serve as key computational and memory storage units in the brain. We discuss both experimental evidence and theoretical models that support this hypothesis and explore its advantages for neuronal function.

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“…Eight groups found evidence consistent with the predictions (McBride et al, 2008, Kleindienst et al, Makino and Malinow, 2011, Chen et al, 2012, Fu et al, 2012, Takahashi et al, 2012, Rah et al, 2013, Druckmann et al, 2014), while two groups did not (Jia et al, 2010, Chen et al, 2011, da Costa and Martin, 2011, Varga et al, 2011). This issue is not resolved and multiple interpretations are still valid (reviewed in DeBello et al, 2014). In experiments where clusters were observed, one consistent finding is inter-synapse distances of ~10 microns or less.…”

Section: Discussionmentioning

confidence: 99%

“…It states that learned information can be stored through spatial clustering of functionally related synaptic inputs on individual branches of dendrite, enabling supralinear summation that strengthens the postsynaptic response. Tests of this idea using diverse techniques and brain systems have recently emerged with heavy emphasis on juvenile brains (reviewed in DeBello et al, 2014) Yet the microstructural changes needed to drive the formation or dissolution of input clusters are observed in both juveniles and adults (Holtmaat and Svoboda, 2009), raising the question of whether such dynamics are harnessed to modify clustering patterns in adults.…”

Section: Introductionmentioning

confidence: 99%

Input clustering in the normal and learned circuits of adult barn owls

McBride

DeBello

2015

Neurobiology of Learning and Memory

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Experience-dependent formation of synaptic input clusters can occur in juvenile brains. Whether this also occurs in adults is largely unknown. We previously reconstructed the normal and learned circuits of prism-adapted barn owls and found that changes in clustering of axo-dendritic contacts (putative synapses) predicted functional circuit strength. Here we asked whether comparable changes occurred in normal and prism-removed adults. Across all anatomical zones, no systematic differences in the primary metrics for within-branch or between-branch clustering were observed: 95–99% of contacts resided within clusters (<10–20 microns from nearest neighbor) regardless of circuit strength. Bouton volumes, a proxy measure of synaptic strength, were on average larger in the functionally strong zones, indicating that changes in synaptic efficacy contributed to the differences in circuit strength. Bootstrap analysis showed that the distribution of inter-contact distances strongly deviated from random not in the functionally strong zones but in those that had been strong during the sensitive period (60d ~ 250d), indicating that clusters formed early in life were preserved regardless of current value. While cluster formation in juveniles appeared to require the production of new synapses, cluster formation in adults did not. In total, these results support a model in which high cluster dynamics in juveniles sculpt a potential connectivity map that is refined in adulthood. We propose that preservation of clusters in functionally weak adult circuits provides a storage mechanism for disused but potentially useful pathways.

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Input clustering and the microscale structure of local circuits

Cited by 37 publications

References 139 publications

A Novel Form of Local Plasticity in Tuft Dendrites of Neocortical Somatosensory Layer 5 Pyramidal Neurons

A Novel Form of Local Plasticity in Tuft Dendrites of Neocortical Somatosensory Layer 5 Pyramidal Neurons

Synaptic clustering within dendrites: An emerging theory of memory formation

Input clustering in the normal and learned circuits of adult barn owls

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