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The Journal of Neuroscience, February 4, 2009, 29(5):1285-1299; doi:10.1523/JNEUROSCI.3728-08.2009

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Behavioral/Systems/Cognitive
Conditional Bursting Enhances Resonant Firing in Neocortical Layer 2–3 Pyramidal Neurons

Matthew H. Higgs^1,2 and William J. Spain^1,2,3

¹Neurology Section, Veterans Affairs Puget Sound Health Care System, Seattle, Washington 98108, and Departments of ²Physiology and Biophysics and ³Neurology, University of Washington, Seattle, Washington 98195

Correspondence should be addressed to William J. Spain, Veterans Affairs Puget Sound Health Care System, Neurology (Mail Stop 127), 1660 South Columbian Way, Seattle, WA 98018. Email: spain{at}u.washington.edu

The frequency response properties of neurons are critical for signal transmission and control of network oscillations. At subthreshold membrane potential, some neurons show resonance caused by voltage-gated channels. During action potential firing, resonance of the spike output may arise from subthreshold mechanisms and/or spike-dependent currents that cause afterhyperpolarizations (AHPs) and afterdepolarizations (ADPs). Layer 2–3 pyramidal neurons (L2–3 PNs) have a fast ADP that can trigger bursts. The present study investigated what stimuli elicit bursting in these cells and whether bursts transmit specific frequency components of the synaptic input, leading to resonance at particular frequencies. We found that two-spike bursts are triggered by step onsets, sine waves in two frequency bands, and noise. Using noise adjusted to elicit firing at 10 Hz, we measured the gain for modulation of the time-varying firing rate as a function of stimulus frequency, finding a primary peak (7–16 Hz) and a high-frequency resonance (250–450 Hz). Gain was also measured separately for single and burst spikes. For a given spike rate, bursts provided higher gain at the primary peak and lower gain at intermediate frequencies, sharpening the high-frequency resonance. Suppression of bursting using automated current feedback weakened the primary and high-frequency resonances. The primary resonance was also influenced by the SK channel-mediated medium AHP (mAHP), because the SK blocker apamin reduced the sharpness of the primary peak. Our results suggest that resonance in L2–3 PNs depends on burst firing and the mAHP. Bursting enhances resonance in two distinct frequency bands.

Key words: burst; resonance; oscillator; frequency; cortex; pyramidal cell

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Received Aug. 6, 2008; revised Dec. 10, 2008; accepted Dec. 10, 2008.

Correspondence should be addressed to William J. Spain, Veterans Affairs Puget Sound Health Care System, Neurology (Mail Stop 127), 1660 South Columbian Way, Seattle, WA 98018. Email: spain{at}u.washington.edu

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