Active dendrites: colorful wings of the mysterious butterflies

doi:10.1016/j.tins.2008.03.004

Trends in Neurosciences

Volume 31, Issue 6, June 2008, Pages 309-316

https://doi.org/10.1016/j.tins.2008.03.004 Get rights and content

Santiago Ramón y Cajal had referred to neurons as the ‘mysterious butterflies of the soul.’ Wings of these butterflies – their dendrites – were traditionally considered as passive integrators of synaptic information. Owing to a growing body of experimental evidence, it is now widely accepted that these wings are colorful, endowed with a plethora of active conductances, with each family of these butterflies made of distinct hues and shades. Furthermore, rapidly evolving recent literature also provides direct and indirect demonstrations for activity-dependent plasticity of these active conductances, pointing toward chameleonic adaptability in these hues. These experimental findings firmly establish the immense computational power of a single neuron, and thus constitute a turning point toward the understanding of various aspects of neuronal information processing. In this brief historical perspective, we track important milestones in the chameleonic transmogrification of these mysterious butterflies.

Section snippets

Background for active dendrites

In 1993, Stuart, Dodt and Sakmann [1] published a landmark paper in which they used a new technique for visualizing neuronal dendrites in living brain slices to record, with whole-cell patch electrodes, action potentials in dendrites of neocortical pyramidal neurons. A year later, Stuart and Sakmann [2] used this technique to make dual recordings from the soma and dendrite of neocortical layer 5 pyramidal neurons and showed unequivocally that action potentials initiated in the axon/soma region

Cataloging properties and functions of active dendrites

The rapid pace of new information about the active properties of dendrites has been largely preceded by the development of new recording and imaging techniques. In addition to methods for direct dendritic recordings mentioned above, the development and use of calcium- and voltage-sensitive indicator dyes and high-speed fluorescence imaging 29, 30, 31 led to a significant advances in our understanding of the active properties of dendrites. More recently, in vivo optical imaging 32, 33, in vivo

Plasticity of active dendrites

What do we mean by plasticity? Plasticity in general means the ability to change or deform and thereby adapt to the environment. In the realm of neuronal plasticity, a neuron or synapse can change its features in response to a stimulus. The changes can take place on a variety of timescales, from the short term (ms) to the very long term (years). The features of a neuron or synapse that can change as a function of its prior history (or be ‘plastic’) are probably limited only by the number of

Concluding remarks

Interest in the functional properties of dendrites and how they participate in synaptic integration, synaptic plasticity, neuronal computations and disease dates back many years, with seminal contributions made by many neuroscientists along the way. It has been and continues to be a major area of research for neuroscience. Many new techniques have been developed for the investigation of dendrites, and these techniques have led to an explosion of new information. From what is currently known, it

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Citation Excerpt :
Classically, LFPs were believed to reflect the synaptic inputs that were received by passive dendritic processes, with the soma as the central processing unit of a neuron (Fig. 1B). While synaptic inputs do play a crucial role in shaping LFPs, it is now well established that dendrites are certainly not mere passive recipients of inputs but express a rich repertoire of active conductances (Magee, 2000; Johnston and Narayanan, 2008; Sjostrom et al., 2008; Spruston, 2008; Narayanan and Johnston, 2012; Nusser, 2012; Major et al., 2013; Stuart and Spruston, 2015) that are equally involved in the processing of inputs and in the genesis and regulation of LFPs (Reimann et al., 2013; Sinha and Narayanan, 2015; Ness et al., 2016, 2018) (Fig. 1C). In this review, we discuss some recent developments in this space at the circuit, cellular, and molecular scales to highlight the complexity involved in the emergence of this gestalt through the presence of active dendrites.
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Trends in Neurosciences

Historical perspectiveReviewActive dendrites: colorful wings of the mysterious butterflies

Section snippets

Background for active dendrites

Cataloging properties and functions of active dendrites

Plasticity of active dendrites

Concluding remarks

Neuroscience

Neuron

J. Neurosci. Methods

Brain Res.

Neuron

Neuron

Neuron

Curr. Opin. Neurobiol.

Neuron

Neuron

Neuron

Biophys. J.

Neuron

Neuron

Curr. Opin. Neurobiol.

Neuron

Neuron

Trends Neurosci.

Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy

Pflugers Arch.

Active propagation of somatic action potentials into neocortical pyramidal cell dendrites

Nature

Electrophysiological properties of dendrites and somata in alligator Purkinje cells

J. Neurophysiol.

Dendritic spikes and their inhibition in alligator Purkinje cells

Science

Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurones in vitro

J. Physiol.

The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function

Science

Foundations of the Neuron Doctrine

Active properties of neuronal dendrites

Annu. Rev. Neurosci.

Die neuroblasten und deren Entstehung im embryonalen Marke

Abhandl. Math.-Phys. Class. Konigl. Sach. Gesellsch. Wiss. Leipzig

Sulla struttura della grigia del cervello

Gazetta Medica Italiana Lombardia

Estructura de los centros nerviosos de las aves

Rev. Trim. Histol. Norm. Patol.

Neuron doctrine and electrophysiology

Science

Comparative physiology of dendrites

The Theoretical Foundation of Dendritic Function

Action potentials of the pyramidal neurones in the hippocampus of the rabbit

J. Physiol.

Interhippocampal impulses II. Apical dendritic activation of CA1 neurons

Acta Physiol. Scand.

Electrophysiological properties of CA1 and CA2 apical dendrites of rabbit hippocampus

J. Neurophysiol.

Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb

J. Neurophysiol.

Electrophysiology of hippocampal neurons. IV. Fast prepotentials

J. Neurophysiol.

Procion yellow electrodes for intracellular recording and staining of neurones in the somatosensory cortex of the rat

J. Physiol.

Intradendritic recordings from hippocampal neurons

Proc. Natl. Acad. Sci. U. S. A.

Electrophysiology of isolated hippocampal pyramidal dendrites

J. Neurosci.

The site for initiation of action potential discharge over the somatodendritic axis of rat hippocampal CA1 pyramidal neurons

J. Neurosci.

Signal enhancement in distal cortical dendrites by means of interactions between active dendritic spines

Proc. Natl. Acad. Sci. U. S. A.

Comparisons between active properties of distal dendritic branches and spines: implications for neuronal computations

J. Cogn. Neurosci.

Cable theory in neurons with active, linearized membranes

Biol. Cybern.

Mapping calcium transients in the dendrites of Purkinje cells from the guinea-pig cerebellum in vitro

J. Physiol.

In vivo dendritic calcium dynamics in neocortical pyramidal neurons

Nature

Imaging cellular network dynamics in three dimensions using fast 3D laser scanning

Nat. Methods

Historical perspective
Review
Active dendrites: colorful wings of the mysterious butterflies