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Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo

Nature volume 503, pages 115–120 (2013)Cite this article

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Abstract

Neuronal dendrites are electrically excitable: they can generate regenerative events such as dendritic spikes in response to sufficiently strong synaptic input1,2,3. Although such events have been observed in many neuronal types4,5,6,7,8,9, it is not well understood how active dendrites contribute to the tuning of neuronal output in vivo. Here we show that dendritic spikes increase the selectivity of neuronal responses to the orientation of a visual stimulus (orientation tuning). We performed direct patch-clamp recordings from the dendrites of pyramidal neurons in the primary visual cortex of lightly anaesthetized and awake mice, during sensory processing. Visual stimulation triggered regenerative local dendritic spikes that were distinct from back-propagating action potentials. These events were orientation tuned and were suppressed by either hyperpolarization of membrane potential or intracellular blockade of NMDA (N-methyl-d-aspartate) receptors. Both of these manipulations also decreased the selectivity of subthreshold orientation tuning measured at the soma, thus linking dendritic regenerative events to somatic orientation tuning. Together, our results suggest that dendritic spikes that are triggered by visual input contribute to a fundamental cortical computation: enhancing orientation selectivity in the visual cortex. Thus, dendritic excitability is an essential component of behaviourally relevant computations in neurons.

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Figure 1: Dendritic patch-clamp recordings from visual cortex pyramidal neurons in vivo.
Figure 2: Visually evoked dendritic burst events are local.
Figure 3: Simultaneous dendritic recording and Ca2+ imaging at the soma shows that dendritic spikes are local.
Figure 4: Hyperpolarization decreases the frequency of dendritic bursts.
Figure 5: Dendritic mechanisms contribute to the selectivity of subthreshold orientation tuning.

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Acknowledgements

We are grateful to B. Clark, P. Latham, M. London, D. Ringach, A. Roth, C. Schmidt-Hieber and C. Wilms for discussions and comments on the manuscript. This work was supported by the following: a Long-Term Fellowship and a Career Development Award from the Human Frontier Science Program and a Klingenstein Fellowship (S.L.S.); a Helen Lyng White Fellowship (I.T.S.); a Wellcome Trust and Royal Society Fellowship and MRC Programme Leader Track (T.B.); and by grants from the Wellcome Trust, ERC and Gatsby Charitable Foundation (M.H.).

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Authors and Affiliations

  1. Wolfson Institute for Biomedical Research and Department of Neuroscience, Physiology and Pharmacology, University College London, Gower Street, London WC1E 6BT, UK,

    Spencer L. Smith, Ikuko T. Smith, Tiago Branco & Michael Häusser

  2. Department of Cell Biology and Physiology and Neuroscience Center, University of North Carolina School of Medicine, Chapel Hill, 27599, North Carolina, USA

    Spencer L. Smith & Ikuko T. Smith

  3. Laboratory of Molecular Biology, Medical Research Council, Cambridge CB2 0QH, UK,

    Tiago Branco

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  1. Spencer L. Smith
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Contributions

S.L.S. and M.H. conceived and designed the experiments. S.L.S. and I.T.S. performed the experiments. S.L.S. analysed the data. T.B. designed and carried out the compartmental modelling. S.L.S., I.T.S., T.B. and M.H. interpreted the data and wrote the paper.

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Correspondence to Spencer L. Smith or Michael Häusser.

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Extended data figures and tables

Extended Data Figure 1 Electrophysiological features of layer 2/3 dendrites in vivo.

a, The input resistance of distal dendrites was typically 100–300 MΩ but sometimes larger (up to 600 MΩ). The input resistance increased as function of dendritic distance from the soma, approximately doubling every 300 µm. The grey point indicates the input resistance measured in somatic patch-clamp recordings (mean ± s.e.m.). b, During a dendritic recording at 150 µm from the soma, hyperpolarizing current steps did not reveal a voltage sag; thus, there is probably little to no hyperpolarization-activated cation current, Ih, in the dendrites of layer 2/3 pyramidal neurons in vivo. c, The peak voltage response plotted against the hyperpolarizing current step amplitude in an I–V plot was well fit by a linear function, confirming the lack of Ih. d, Representative dendritic bursts evoked by visual stimulation at the optimal orientation in nine different dendritic recordings at progressively increasing distances from the soma. All right-hand scale bars are 20 mV. e, f, Compared with action potentials recorded at the soma, bAPs had a lower amplitude (e) and were prolonged in time (f), and both of these trends were more pronounced with increasing dendritic distance from the soma (error bars, s.d.). Both the amplitude and width were significantly different among the three groups (P < 0.01, unpaired t-tests with the Bonferroni correction for multiple comparisons).

Extended Data Figure 2 Orientation tuning curves of dendritic bursts compared with bAPs.

Tuning curves for dendritic spike bursts and bAPs recorded at distal dendritic locations (>75 µm from soma) are shown. The tuning curves for dendritic bursts match the tuning curves for isolated bAPs. The statistical significance of dendritic burst tuning curves was tested by randomly shuffling responses (details in the Methods) and was found to be significant (P < 0.05) for 7 out of 9 cells (dendritic burst tuning in cells 6 and 9 was not significant). The curves were normalized to the maximal values, which are shown at the bottom right of each polar plot. The small qualitative differences may be due to dendrites that are topologically distant from the dendritic recording site exhibiting slightly different tuning curves. The grating drift direction that elicited the largest response is indicated with an arrow. The difference between these directions is indicated at the bottom of each polar plot. The cross correlation between dendritic bursts and isolated bAPs was highly significant: Pearson’s R = 0.54, P = 0.000013, paired t-test; n = 9. When only the spikes in the bursts with rise times in the slowest quartile of the distribution were considered to be dendritic in origin, the preferred orientation of bAPs and the slowest quartile were still matched within individual dendritic recordings (difference in preferred orientation, 41.5 ± 58.1°; P = 0.49, paired t-test; n = 9).

Extended Data Figure 3 Dendritic recordings in awake mice exhibit dendritic bursts.

a, Awake, head-fixed mice viewed drifting gratings during electrophysiological recordings. b, A two-photon image of the patched dendrite (117 µm from the soma) of a layer 2/3 pyramidal neuron in the mouse visual cortex, after filling with Alexa Fluor 594 with the dendritic patch-clamp pipette. c, Dendritic bursts were observed when the preferred orientation was presented. d, Tuning curves for the isolated bAPs and dendritic bursts. e, Example bursts from three different distal dendritic recordings in awake mice. Calibration bars, 25 mV.

Extended Data Figure 4 The diversity of onset dynamics versus membrane potential.

a, Spikes from each distal dendritic recording (both isolated bAPs (black) and spikes in dendritic burst events (red)) were normalized such that isolated bAPs had a mean phase slope of 1. The mean baseline membrane potential (Vm) of isolated bAPs was subtracted from the mean baseline Vm of all spikes. Although many spikes in bursts had a depolarized baseline Vm relative to isolated spikes, there was overlap between the two populations around ±3 mV. b, Magnification of panel a to show spikes at ±3 mV relative to the mean baseline Vm of isolated bAPs. c, Histograms of the two populations reveal a tendency towards lower phase slope values for spikes in bursts (P = 0.041, Kolmogorov–Smirnov test ; n = 211 bAPs, 80 spikes in bursts). d, An example of bAPs and a spike in a burst (both from the same distal dendritic recording): although the bAP has a more depolarized baseline Vm, it still exhibits a steeper phase slope (a kink at the foot of the voltage waveform), indicative of a propagated action potential.

Extended Data Figure 5 Ca2+ imaging at the site of dendritic recording reveals that global Ca2+ signals are associated with faster onset spikes.

a, During dendritic recordings, Ca2+ signals were simultaneously imaged at the site of the recording and at nearby dendrites. b, In dendritic bursts with global Ca2+ signals that were simultaneously observed in all regions of interest (ROIs), the spikes recorded at the dendrite exhibited steep onsets, indicating that they were probably bAPs. c, In local Ca2+ signals that were observed only in the ROI at the site of recording, the dendritic spikes exhibited slower onsets, indicating that they were probably locally generated. d, The maximum phase slope of spikes occurring during global Ca2+ events was higher than for spikes occurring during local Ca2+ events (P = 0.0069, t-test). e, f, When global Ca2+ signals occurred during ongoing local Ca2+ signals, the initiation was associated with a steep onset spike. Two examples are shown.

Extended Data Figure 6 Non-firing cells exhibit subthreshold orientation tuning.

a, Raw data for an example cell in which subthreshold orientation tuning was observed, although no spikes were fired during stimulus presentations. b, In this case, the tuning width of the subthreshold membrane potential was quite sharp and was confined to two directions.

Extended Data Figure 7 Tuning of action potentials and subthreshold membrane potential.

a, In individual cells, the orientation tuning of spikes and the membrane potential were highly correlated, indicating that the tuning of the subthreshold responses was not spurious (mean difference in preferred orientation, 14.8 ± 5.3°). b, In individual cells, the orientation selectivity index based on the membrane potential response (VmOSI) was highly correlated with the conventional spiking-based OSI. c, In individual cells, the preferred orientation of the control subthreshold response was correlated with the preferred orientation of the subthreshold response during hyperpolarization. d, The black curve is the fitted subthreshold orientation tuning curve (the black circles are raw data points), and the red curve is the subthreshold tuning curve during hyperpolarization (the red circles are raw data points). The VmOSI values for the control and hyperpolarized conditions are shown next to each plot. The radial axes are linear and start at 0. The maximal radial axis range is shown below each polar plot. The differences in VmOSI are quantified in Fig. 5g.

Extended Data Figure 8 Changes in the driving force for Cl−do not account for the effects of hyperpolarization on VmOSI.

a, When the pipette solution contained 10 mM Cl−, the reversal potential for chloride, ECl, was estimated to be −71 mV (based on the assumption that natural cerebrospinal fluid contains a similar amount of Cl− to the artificial cerebrospinal fluid used). In this situation, hyperpolarization decreased the orientation selectivity index. b, Even with a low Cl− concentration (4 mM; estimated ECl, −95 mV), the result was the same. c, There was no significant correlation between the driving force for Cl− and VmOSI. d, The data were resampled (15 of the data points in c were selected at random, and the R and P values for that set of data points were calculated; this process was repeated 10,000 times), and this process confirmed that the result from the correlational analysis in c was not biased by a small subset of the data points (the mean R and P values from the resampling analysis match the values for the full data set in c well).

Extended Data Figure 9 The effect of intracellular MK-801 on up and down states and dendritic spikes.

a, To determine whether MK-801 that might have leaked out of the pipette during patching affects network circuitry, we examined the dynamics of up and down states in recordings in which MK-801 was in the pipette and in control recordings (no MK-801). b, Although, in general, the membrane potential drifted up slightly (<5 mV on average) and the time spent in the up state increased over long recordings (possibly due to the anaesthesia wearing off), these trends were identical with or without MK-801 in the patch pipette. c, When 1 µM MK-801 was included in the recording pipette, the visually evoked responses contained fewer bAPs and bursts. This trend was clear in individual cells (a) and across the population (d). This reduction in spiking confirms that dendritic bursts do not occur when NMDA receptors are blocked. Because the low firing rate in MK-801 recordings prevented a reliable measurement of orientation tuning in the MK-801 dendritic patch-clamp recordings, we averaged over all of the stimulus presentations for both conditions, resulting in a lower average firing rate for bAPs and dendritic bursts.

Extended Data Figure 10 Compartmental modelling of dendritic events.

a, A detailed reconstruction of a layer 2/3 pyramidal cell was used in the simulations. Light green circles over the dendritic tree represent background synapses, and dark green circles represent signal synapses (the model had 1,100 synapses; not all are illustrated). Voltage was recorded at the soma and at all dendritic branches simultaneously. b, Activation of signal synapses at 5 Hz produced high-frequency dendritic bursts, composed of local dendritic spikes and bAPs. These bursts were always accompanied by dendritic Ca2+ transients. The timing of the activation of excitatory synapses on the recorded dendritic branch is illustrated. Note how the local excitatory postsynaptic potentials (EPSPs) are clearly smaller than the dendritic spikes. c, Examples of specific features consistently observed in the model. Isolated bAPs were associated with global Ca2+ transients and had kinked onsets. Dendritic spikes often preceded somatic action potentials, had smooth onsets and Ca2+ transients that were localized to the branches where the spikes were recorded, and clearly started before the global transients associated with bAPs. Local dendritic spikes initiated in the dendrite could often be recorded in multiple electrotonically close dendritic branches. Pairs of local spikes and bAPs reached very high frequencies; the example shows a pair at >400 Hz. When NMDA receptors were removed from the simulations, no dendritic spikes were observed, and the soma failed to reach the threshold for action potential firing. This also occurred when there were no dendritic voltage-activated Na+ channels, indicating that the generation of dendritic spikes is required for producing axonal output. d, Quantification of spike onset for local dendritic spikes and bAPs in the model reproduced the experimentally observed effect reported in Extended Data Fig. 5d. e, Example trial showing the somatic voltage and recordings for two dendrites indicated in a. For each dendrite, the local voltage, the Na+ channel conductance (gNa, expressed as a fraction of the maximum conductance) and the timing of activation of excitatory synapses on the recorded dendrite are shown. The gNa traces show that there is significant local Na+ channel inactivation after the first spike and that subsequent spikes are associated with varying degrees of Na+ channel conductance. Asterisks denote extreme cases when a bAP followed a local dendritic spike at very high frequency and did not recruit any local gNa, thereby indicating that the propagation into the recorded branch was passive.

Supplementary information

Supplementary Information

This file contains a Supplementary Note and additional references. This file was replaced on 6 November 2013. (PDF 206 kb)

The propagation of voltage in the compartmental model during synaptic activation

Background input was continuously active, and signal synapses were activated at 8 Hz for 200 ms (100 ms after the start of the trace). The traces show the local voltage at the indicated dendrites, together with the somatic voltage. During the period of high synaptic input local dendritic spikes are elicited in multiple regions of the dendritic tree, and eventually lead to a somatic action potential the backpropagates globally. Note how all of the global spikes are preceded by at least one dendritic spike in a region of the dendritic tree. (MOV 5410 kb)

Slow motion video of the same trial shown in Video 1, highlighting the activity in dendrite 3

Note that the first two global spikes are immediately preceded by local spikes in this dendrite, and that while the last dendritic spike does not directly trigger a somatic action potential it leads to a significant charge build up in the soma that facilitates the subsequent somatic firing. (MOV 3761 kb)

Slow motion video of the same trial shown in Video 1, highlighting the activity in dendrite 1

Note that dendrite 1 fires bursts of spikes at frequencies >50 Hz. (MOV 3793 kb)

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Smith, S., Smith, I., Branco, T. et al. Dendritic spikes enhance stimulus selectivity in cortical neurons in vivo . Nature 503, 115–120 (2013). https://doi.org/10.1038/nature12600

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