Dendritic backpropagation and the state of the awake neocortex - PubMed (original) (raw)

Dendritic backpropagation and the state of the awake neocortex

Yulia Bereshpolova et al. J Neurosci. 2007.

Abstract

The spread of somatic spikes into dendritic trees has become central to models of dendritic integrative properties and synaptic plasticity. However, backpropagating action potentials (BPAPs) have been studied mainly in slices, in which they are highly sensitive to multiple factors such as firing frequency and membrane conductance, raising doubts about their effectiveness in the awake behaving brain. Here, we examine the spatiotemporal characteristics of BPAPs in layer 5 pyramidal neurons in the visual cortex of adult, awake rabbits, in which EEG-defined brain states ranged from alert vigilance to drowsy/inattention, and, in some cases, to light sleep. To achieve this, we recorded extracellular spikes from layer 5 pyramidal neurons and field potentials above and below these neurons using a 16-channel linear probe, and applied methods of spike-triggered current source-density analysis to these records (Buzsáki and Kandel, 1998; Swadlow et al., 2002). Precise retinotopic alignment of superficial and deep cortical sites was used to optimize alignment of the recording probe with the axis of the apical dendrite. During the above network states, we studied BPAPs generated spontaneously, antidromically (from corticotectal neurons), or via intense synaptic drive caused by natural visual stimulation. Surprisingly, the invasion of BPAPs as far as 800 microm from the soma was little affected by the network state and only mildly attenuated by high firing frequencies. These data reveal that the BPAP is a robust and highly reliable property of neocortical apical dendrites. These events, therefore, are well suited to provide crucial signals for the control of synaptic plasticity during information-processing brain states.

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Figures

Figure 1.

Figure 1.

The method for extracellular detection of BPAPs. A, The recording situation. Extracellular somatic spikes were recorded from neurons in layer 5 of V1 of awake rabbits, using one of the recording sites on a 16-channel, vertically oriented linear probe (100 μm spacing; top). Field potentials were recorded from each of the probe sites. Vertical alignment of the probe was guided by simultaneous mapping of visual receptive fields at several recording sites through the cortical layers (blue, green, and red arrows), and the angle of the probe was adjusted until we achieved near-perfect retinotopic alignment (bottom; thick contour lines represent the peak receptive field response, and thin lines indicate contour of the response at 30% of maximum). B1, Spike-triggered averaging of the field potentials above the somatic recording sites reveals gradually decaying spikes, which are time locked with the somatic spike but with a progressively increasing latency. B2, B3, CSD analysis of the voltage traces delineates a short-duration current sink propagating vertically. The black filled areas in B2 denote current sinks. C, No such backpropagation was seen after the spikes of putative cortical fast-spike interneurons. In all figures, vertical dashed brackets indicate our estimate of the position of layer 4, and the horizontal arrow indicates the recording site of the spike that triggered the CSD profile. Color coding for CSD traces: here, and in subsequent figures, red indicates current sink, and blue indicates source.

Figure 2.

Figure 2.

The effect of firing frequency on the BPAP. A, Reduction in BPAPs during high-frequency (200 Hz) antidromic activation. Four stimuli are delivered to the superior colliculus (vertical arrows). Open arrows mark the same depth for BPAPs resulting from the first and fourth antidromic spikes in the train for comparison. B, Examples of spike-triggered averaged CSD selected by the interval from the preceding spike (marked above), revealing faster decay for the shorter intervals. C, Summary diagram of the BPAP decays with distance from the soma for different preceding intervals, measured from the spike-triggered averaged CSD and normalized to the somatic spike. Data from 10 neurons are expressed as mean ± SEM. The inset displays the relationship between the slopes of the linear fits to the decay curves and the mid-bin ISI, revealing strong correlation for frequencies higher than 10 Hz.

Figure 3.

Figure 3.

BPAPs evoked during sensory drive. A1–A3, Example of a BPAP from a neuron stimulated by drifting visual grating, during the trough of activity (A1), the peak of activity (A2), or during spontaneous firing (A3). Note the intense synaptic response evident in the CSD in A2. The vertical brackets mark the three recording sites used for quantitative comparison below. Recordings from more distal sites were obscured by the strong field potential generated by sensory stimulation. B, Histogram of the average response to one cycle in the visual stimulation. The periods used for analysis are denoted by horizontal bars. C, Comparison of the amplitude of the BPAPs at the three recording sites and during the same periods shown in A1 and A2.

Figure 4.

Figure 4.

BPAPs evoked during electrically evoked inhibition. A, Poststimulus time histograms of the response to callosal stimulation. The top presents multiunit activity from a supragranular electrode site, demonstrating short increase followed by a strong reduction of firing rate. The bottom is from a deeper site, from the CTect neuron studied in B, which responded only with prolonged inhibition to callosal stimulation. Inhibition (reduced responding) is seen in the multiunit record throughout the depths of the cortex at intervals of 30–150 ms after callosal stimulation. The dotted line delineates the timing of the tectal (antidromic) stimulation shown in B. B, Electrical stimulation of the superior colliculus 30 ms after the callosal stimulus resulted in an antidromic response 3.3 ms later, during the cortical inhibitory period generated by the callosal stimulus. The resulting BPAP (displayed) is virtually identical to that seen without the callosal stimulus. The oblique dotted lines denote what are probably antidromically elicited BPAPs from other (more distant) CTect neurons. C, Plot of the decay curves of the BPAP for the same cell as in B, at different time points after the callosal stimulus, and for antidromic spikes evoked with no preceding callosal stimulation (red). CC, Corpus callosum.

Figure 5.

Figure 5.

BPAPs during EEG-defined brain states. Specific EEG states (shown below) were identified via recordings from the hippocampus (Hipp), primary somatosensory (S1), and V1 cortex. A–D, The BPAPs shown resulted from spikes that occurred during alert vigilance (A), an awake, non-alert state (B), during cortical sleep spindles (C), and during interspindle intervals (D). The last two stages are typical of light sleep. E, Average decay curves of BPAPs from five neurons during the four states as above. Data are expressed as mean ± SEM of the CSD amplitude normalized to the somatic value.

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