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The Journal of Neuroscience, August 29, 2007, 27(35):9392-9399; doi:10.1523/JNEUROSCI.2218-07.2007

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Behavioral/Systems/Cognitive
Dendritic Backpropagation and the State of the Awake Neocortex

Yulia Bereshpolova,¹ Yael Amitai,^1,2 Alexander G. Gusev,¹ Carl R. Stoelzel,¹ and Harvey A. Swadlow¹

¹Department of Psychology, University of Connecticut, Storrs, Connecticut 06269, and ²Department of Physiology, Ben-Gurion University, Beer-Sheva 84105, Israel

Correspondence should be addressed to Harvey A. Swadlow, Department of Psychology, University of Connecticut, 406 Babbidge Road, Unit 1020, Storrs, CT 06269-1020. Email: harvey.swadlow{at}uconn.edu

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 µm 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.

Key words: corticotectal neurons; fast-spiking neurons; apical dendrites; CSD; spike-triggered averaging; dendritic integration

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Received May 15, 2007; revised July 3, 2007; accepted July 11, 2007.

Correspondence should be addressed to Harvey A. Swadlow, Department of Psychology, University of Connecticut, 406 Babbidge Road, Unit 1020, Storrs, CT 06269-1020. Email: harvey.swadlow{at}uconn.edu

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