Computational subunits in thin dendrites of pyramidal cells

Polsky, Aloan; Mel, Bartlett W.; Schiller, Jackie

doi:10.1038/nn1253

Cited by 735 publications

(792 citation statements)

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“…For instance, local spikes (Golding and Spruston 1998;Kamondy et al 1998;Masukawa and Prince 1984;Regher et al 1993; this report) are a well-established electrogenic event whose integrative rules shall prevail over those of the elementary synaptic inputs from which they were born out. The debate on sub-or supralinear summation of distal inputs at the somato-axonic triggering area (e.g., Cash and Yuste 1999;Polsky et al 2004) should be translated to the nearest location at the distal end of the apical shaft because the present experimental results and previous computational studies (López-Aguado et al 2002) do indicate that, once the AP is initiated in this structure, cell output is ensured.…”

Section: Discussionmentioning

confidence: 81%

Synaptically Recruited Apical Currents Are Required to Initiate Axonal and Apical Spikes in Hippocampal Pyramidal Cells: Modulation by Inhibition

Canals

López-Aguado²,

Herreras³

2005

Journal of Neurophysiology

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Canals, S., L. López-Aguado, and O. Herreras. Synaptically recruited apical currents are required to initiate axonal and apical spikes in hippocampal pyramidal cells: modulation by inhibition. J Neurophysiol 93: 909 -918, 2005. First published September 29, 2004; doi:10.1152/jn.00686.2004. Dendritic voltage-dependent currents and inhibition modulate the information flow between synaptic and decision areas. Subthreshold and spike currents are sequentially recruited by synaptic potentials in the apical shaft of pyramidal cells, which may also decide cell output. We studied the global role of proximal apical recruited currents on cell output in vitro and in the anesthetized rat after local blockade of Na ϩ currents in the axon initial segment (AIS) or the proximal apical shaft and their modulation by inhibition. Microejection of TTX, field potentials, and intrasomatic and intradendritic recordings were employed. Dendritic population spikes (PSs) were much smaller in vitro, but the gross relations between synaptic and active currents are similar to in vivo. Activation of Schaffer collaterals triggered PSs and action potentials (APs) in the apical shaft that fully propagated to the axon. However, the specific blockade of proximal Na ϩ currents avoided cell firing, although antidromic PSs and APs readily invaded somata. The somatic depolarization of subthreshold excitatory postsynaptic potentials (EPSPs) also decreased to about 50%. These results were not due to decreased excitatory input by TTX. However, when GABA A inhibition was locally removed, Schaffer synaptic currents skipped the proximal dendrite and fired somatic PSs, although initiated at the AIS. It is concluded that apical currents recruited en passant by Schaffer synaptic potentials in the apical shaft constitute a necessary amplifier for this input to cause output decision. Local inhibition decides when and where an AP will initiate, constituting an efficient mechanism to discriminate and weight different inputs. I N T R O D U C T I O NDendritic voltage-dependent currents participate in basic neuron functions as the conduction of action potentials (APs) and the plastic events born out of their local interaction with synaptic currents (Johnston et al. 1996;Reyes 2001). Less is known on their role on the forward transmission of inputs. They are involved on the reshaping of the excitatory and inhibitory postsynaptic potentials (EPSPs/IPSPs), and the initiation of local spikes (Herreras 1990;Lipowsky et al. 1996;Magee and Johnston 1995;Martina et al. 2000;Stuart and Sakmann 1995;Williams and Stuart 2003). The apical shaft collects all apical inputs and may thus modulate and convey to the axon initial segment (AIS) an integrated signal separated from basal inputs. Whether local spikes on secondary branches will propagate or not into and beyond the apical shaft depends on a number of factors including its geometry, active properties, and specific local inhibition. Recently, we showed that this structure has a suitable geometry for safe forward conduction of A...

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Section: Discussionmentioning

confidence: 81%

Synaptically Recruited Apical Currents Are Required to Initiate Axonal and Apical Spikes in Hippocampal Pyramidal Cells: Modulation by Inhibition

Canals

López-Aguado²,

Herreras³

2005

Journal of Neurophysiology

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“…The simplicity of the IF model contrasts with the complexity of the dendritic arborization of some pyramidal neurons, with their regenerative membrane currents and clustered synaptic inputs (Spruston 2008). The extended geometry of cortical neurons and their nonlinear dentritic properties may offer additional computational power by exploiting nonlinear dendritic properties (Poirazi et al 2003;Polsky et al 2004), like the multiplicative gain modulation of the somatic response function reviewed here.…”

Section: Discussionmentioning

confidence: 99%

The response of cortical neurons to in vivo-like input current: theory and experiment: II. Time-varying and spatially distributed inputs

et al. 2008

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The response of a population of neurons to time-varying synaptic inputs can show a rich phenomenology, hardly predictable from the dynamical properties of the membrane's inherent time constants. For example, a network of neurons in a state of spontaneous activity can respond significantly more rapidly than each single neuron taken individually. Under the assumption that the statistics of the synaptic input is the same for a population of similarly behaving neurons (mean field approximation), it is possible to greatly simplify the study of neural circuits, both in the case in which the statistics of the input are stationary (reviewed in La Camera et al. in Biol Cybern, 2008) and in the case in which they are time varying and unevenly distributed over the dendritic tree. Here, we review theoretical and experimental results on the single-neuron properties that are relevant for the dynamical collective behavior of a population of neurons. We focus on the response of integrate-and-fire neurons and real cortical neurons to long-lasting, noisy, in vivo-like stationary inputs and show how the theory can predict the observed rhythmic activity of cultures of neurons. We then show how cortical neurons adapt on multiple time scales in response to input with stationary statistics in vitro. Next, we review how it is possible to study the general response properties of a neural circuit to time-varying inputs by estimating the response of single neurons to noisy sinusoidal currents. Finally, we address the dendrite-soma interactions in cortical neurons leading to gain modulation and spike bursts, and show how these effects can be captured by a two-compartment integrate-and-fire neuron. Most of the experimental results reviewed in this article have been successfully reproduced by simple integrate-and-fire model neurons.

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“…(e) Data analysis figure 1a), and two synaptic shocks were delivered in the vicinity of a basal dendrite [6,13]. The mean peak amplitude of the NMDA spike in somatic recordings (figure 1b, patch, NMDA spike) was 11.5 + 0.6 mV (n ¼ 51 measurements in eight cells).…”

Section: (D) Drugsmentioning

confidence: 99%

Contribution of extrasynapticN-methyl-d-aspartate and adenosine A1 receptors in the generation of dendritic glutamate-mediated plateau potentials

Oikonomou

Singh

Rich

et al. 2015

Phil. Trans. R. Soc. B

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One contribution of 16 to a discussion meeting issue 'Release of chemical transmitters from cell bodies and dendrites of nerve cells'. Thin basal dendrites can strongly influence neuronal output via generation of dendritic spikes. It was recently postulated that glial processes actively support dendritic spikes by either ceasing glutamate uptake or by actively releasing glutamate and adenosine triphosphate (ATP). We used calcium imaging to study the role of NR2C/D-containing N-methyl-D-aspartate (NMDA) receptors and adenosine A1 receptors in the generation of dendritic NMDA spikes and plateau potentials in basal dendrites of layer 5 pyramidal neurons in the mouse prefrontal cortex. We found that NR2C/D glutamate receptor subunits contribute to the amplitude of synaptically evoked NMDA spikes. Dendritic calcium signals associated with glutamate-evoked dendritic plateau potentials were significantly shortened upon application of the NR2C/D receptor antagonist PPDA, suggesting that NR2C/D receptors prolong the duration of calcium influx during dendritic spiking. In contrast to NR2C/D receptors, adenosine A1 receptors act to abbreviate dendritic and somatic signals via the activation of dendritic K þ current. This current is characterized as a slow-activating outward-rectifying voltage-and adenosine-gated current, insensitive to 4-aminopyridine but sensitive to TEA. Our data support the hypothesis that the release of glutamate and ATP from neurons or glia contribute to initiation, maintenance and termination of local dendritic glutamate-mediated regenerative potentials.

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Computational subunits in thin dendrites of pyramidal cells

Cited by 735 publications

References 42 publications

Synaptically Recruited Apical Currents Are Required to Initiate Axonal and Apical Spikes in Hippocampal Pyramidal Cells: Modulation by Inhibition

Synaptically Recruited Apical Currents Are Required to Initiate Axonal and Apical Spikes in Hippocampal Pyramidal Cells: Modulation by Inhibition

The response of cortical neurons to in vivo-like input current: theory and experiment: II. Time-varying and spatially distributed inputs

Contribution of extrasynapticN-methyl-d-aspartate and adenosine A1 receptors in the generation of dendritic glutamate-mediated plateau potentials

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