Synaptic Depolarization Is More Effective than Back-Propagating Action Potentials during Induction of Associative Long-Term Potentiation in Hippocampal Pyramidal Neurons

Hardie, Jason B.; Spruston, Nelson

doi:10.1523/jneurosci.6000-08.2009

Cited by 74 publications

(75 citation statements)

References 42 publications

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“…It is well known that pairing of presynaptic spikes with postsynaptic depolarization is often sufficient for the induction of LTP, i.e., a postsynaptic somatic spike is not necessary (Kelso et al, 1986;Gustafsson et al, 1987;Hardie and Spruston, 2009). We model LTP in the absence of postsynaptic somatic spiking by the following weight dynamics:…”

Section: Plasticity Mechanismsmentioning

confidence: 99%

“…It is well known, however, that pairing of presynaptic spikes with postsynaptic depolarization can be sufficient for the induction of LTP (Kelso et al, 1986;Gustafsson et al, 1987;Hardie and Spruston, 2009). In our model, synapses can also be somewhat potentiated in the absence of postsynaptic firing and dendritic spikes, although potentiation in the presences of a dendritic spike is substantially stronger because the amount of potentiation increases linearly with the local branch depolarization b k (see Eq.…”

Section: Synaptic Plasticity and Branch-strength Potentiationmentioning

confidence: 99%

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Branch-Specific Plasticity Enables Self-Organization of Nonlinear Computation in Single Neurons

Legenstein¹,

Maass²

2011

Journal of Neuroscience

162

152

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It has been conjectured that nonlinear processing in dendritic branches endows individual neurons with the capability to perform complex computational operations that are needed to solve for example the binding problem. However, it is not clear how single neurons could acquire such functionality in a self-organized manner, because most theoretical studies of synaptic plasticity and learning concentrate on neuron models without nonlinear dendritic properties. In the meantime, a complex picture of information processing with dendritic spikes and a variety of plasticity mechanisms in single neurons has emerged from experiments. In particular, new experimental data on dendritic branch strength potentiation in rat hippocampus have not yet been incorporated into such models. In this article, we investigate how experimentally observed plasticity mechanisms, such as depolarization-dependent spike-timing-dependent plasticity and branch-strength potentiation, could be integrated to self-organize nonlinear neural computations with dendritic spikes. We provide a mathematical proof that, in a simplified setup, these plasticity mechanisms induce a competition between dendritic branches, a novel concept in the analysis of single neuron adaptivity. We show via computer simulations that such dendritic competition enables a single neuron to become member of several neuronal ensembles and to acquire nonlinear computational capabilities, such as the capability to bind multiple input features. Hence, our results suggest that nonlinear neural computation may self-organize in single neurons through the interaction of local synaptic and dendritic plasticity mechanisms.

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Section: Plasticity Mechanismsmentioning

confidence: 99%

Section: Synaptic Plasticity and Branch-strength Potentiationmentioning

confidence: 99%

Branch-Specific Plasticity Enables Self-Organization of Nonlinear Computation in Single Neurons

Legenstein¹,

Maass²

2011

Journal of Neuroscience

162

152

View full text Add to dashboard Cite

show abstract

“…For example, strong stimulation to one set of synapses can result in LTP in those synapses as well as in a separate, weakly stimulated set of synapses when the weak stimulation alone does not generate LTP (Hardie & Spruston, 2009). Our simulations demonstrate that due to the voltage dependence of NMDA channels and VGCCs, when dendritic depolarisation increases as more synapses are stimulated synchronously, the pCa levels in each spine head rise as well.…”

Section: Stimulation Of Single Dendritic Layersmentioning

confidence: 99%

“…This illustrates the cooperativity among synapses that may underpin the cooperativity known to influence plasticity. It is a clear demonstration of the importance of dendritic depolarization, regardless of somatic spiking and backpropagation of action potentials, in determining synaptic plasticity (Hardie & Spruston, 2009).…”

Section: Stimulation Of Single Dendritic Layersmentioning

confidence: 99%

Spine Head Calcium as a Measure of Summed Postsynaptic Activity for Driving Synaptic Plasticity

2014

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We use a computational model of a hippocampal CA1 pyramidal cell to demonstrate that spine head calcium provides an instantaneous readout at each synapse of the postsynaptic weighted sum of all presynaptic activity impinging on the cell. The form of the readout is equivalent to the functions of weighted, summed inputs used in neural network learning rules. Within a dendritic layer, peak spine head calcium levels are either a linear or sigmoidal function of the number of coactive synapses, with nonlinearity depending on the ability of voltage spread in the dendrites to reach calcium spike threshold. This is strongly controlled by the potassium A-type current, with calcium spikes and the consequent sigmoidal increase in peak spine head calcium present only when the A-channel density is low. Other membrane characteristics influence the gain of the relationship between peak calcium and the number of active synapses. In particular, increasing spine neck resistance increases the gain due to increased voltage responses to synaptic input in spine heads. Colocation of stimulated synapses on a single dendritic branch also increases the gain of the response. Input pathways cooperate: CA3 inputs to the proximal apical dendrites can strongly amplify peak calcium levels due to weak EC input to the distal dendrites, but not so strongly vice versa. CA3 inputs to the basal dendrites can boost calcium levels in the proximal apical dendrites, but the relative electrical compactness of the basal dendrites results in the reverse effect being less significant. These results give pointers as to how to better describe the contributions of pre-and Spine Head Calcium Driving Synaptic Plasticity 2195 postsynaptic activity in the learning "rules" that apply in these cells. The calcium signal is closer in form to the activity measures used in traditional neural network learning rules than to the spike times used in spike-timing-dependent plasticity.

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“…Further studies provided evidence that these associative interactions are most effective when the two inputs terminate in spatially-overlapping regions of the dendritic tree (Hardie and Spruston, 2009;White et al, 1988White et al, , 1990 or individual branches (Govindarajan et al, 2011), although there is one report that strong stimulation of a basal dendritic (s. oriens) input can facilitate LTP in a simultaneously-stimulated apical dendritic input (Gustafsson and Wigstrom, 1986). We investigated associative interactions between basal and apical dendritic synapses using TBS in field CA1 of hippocampal slices from adult male CD-1 mice, prepared and maintained as described above.…”

mentioning

confidence: 99%

Cellular Basis for Learning Impairment in Fragile X Syndrome

Larson¹

2014

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Public reporting burden for this collection of information is estimated to average 1 hour per response, including the time for reviewing instructions, searching existing data sources, gathering and maintaining the data needed, and completing and reviewing this collection of information. Send comments regarding this burden estimate or any other aspect of this collection of information, including suggestions for reducing this burden to Department of Defense, Washington Headquarters Services, Directorate for Information , 1215 Jefferson Davis Highway, Suite 1204, Arlington, VA 22202-4302. Respondents should be aware that notwithstanding any other provision of law, no person shall be subject to any penalty for failing to comply with a collection of information if it does not display a currently valid OMB control number. PLEASE DO NOT RETURN YOUR FORM TO THE ABOVE ADDRESS. REPORT DATE August 2014 REPORT TYPE PERFORMING ORGANIZATION NAME(S) AND ADDRESS(ES)University of Illinois at Chicago PERFORMING ORGANIZATION REPORT NUMBERChicago, IL 60612-4305 SPONSORING / MONITORING AGENCY NAME(S) AND ADDRESS(ES) 10. SPONSOR/MONITOR'S ACRONYM(S) U.S. Army Medical Research and Materiel Command Fort Detrick, Maryland 21702-5012 SPONSOR/MONITOR'S REPORT NUMBER(S) DISTRIBUTION / AVAILABILITY STATEMENTApproved for Public Release; Distribution Unlimited SUPPLEMENTARY NOTES ABSTRACTThis research combines behavioral, electrophysiological, and molecular approaches to elucidate the cellular basis for learning impairment in Fragile X Syndrome (FXS), using olfactory learning in Fmr1-KO mice as a model system. We hypothesize that FMRP, the protein missing in FXS, participates in two aspects of circuit function that are critical to learning: synaptic plasticity and the generation and survival of new neurons in the adult brain. Efforts in the second year of support were directed toward establishing a method to specifically upregulate neurogenesis in adult fragile X mice, test fragile X mice for learning deficits in hippocampal-independent tasks, and determine if learning affects NMDA receptor trafficking to synapses. Significant advances have been made in the establishment of behavioral paradigms to test both hippocampal -dependent and -independent forms of olfactory learning. Experimental paradigms have also been refined for the study of neurogenesis in the olfactory bulb, glutamate receptor expression as it relates to olfactory learning in olfactory cortex and hippocampus, and the effects of aging on glutamate receptor expression. These studies are likely to advance our understanding of intellectual disability and autism in addition to the specific condition of fragile X syndrome. This knowledge will be necessary for the development of rational strategies for prevention and treatment of cognitive impairments from a variety of causes. SUBJECT TERMSFragile X Syndrome, synaptic plasticity, long-term potentiation, glutamate receptors, neurogenesis, olfactory learning INTRODUCTIONFragile X syndrome is the most common inherited form of intellect...

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Synaptic Depolarization Is More Effective than Back-Propagating Action Potentials during Induction of Associative Long-Term Potentiation in Hippocampal Pyramidal Neurons

Cited by 74 publications

References 42 publications

Branch-Specific Plasticity Enables Self-Organization of Nonlinear Computation in Single Neurons

Branch-Specific Plasticity Enables Self-Organization of Nonlinear Computation in Single Neurons

Spine Head Calcium as a Measure of Summed Postsynaptic Activity for Driving Synaptic Plasticity

Cellular Basis for Learning Impairment in Fragile X Syndrome

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