Neuronal biophysics modulate the ability of gamma oscillations to control
response timing.
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1
Salk Institute for Biological Studies, Crick-Jacobs Center, United States
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2
Salk Institute, United States
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3
UCSD Neuroscience Graduate Program, United States
Gamma frequency oscillatory activity of inhibitory sub-networks has been hypothesized to regulate information processing in the cortex as a whole. Inhibitory neurons in these sub-networks synchronize their firing and selectively innervate the perisomatic compartments of their target neurons, generating both tonic and rapidly fluctuating inhibition that is hypothesized to enforce temporal precision and coordinate the activity of their post-synaptic targets. Indeed, in vivo and in vitro recordings have demonstrated that many neurons’ firing is entrained to these oscillations, although to varying extents and at various phases. Cortical networks are composed of diverse populations of cells that differ in their chemical content, biophysical characteristics, laminar location, and connectivity. Thus, different types of neurons may vary in the amplitude and timing of the synchronized inhibition they receive, as well as in the effects of pattern of inhibitory inputs on response timing and precision. What accounts for this heterogeneity of response timing between cell types, and are these response properties fixed or flexible? To answer these questions, we use a combination of in vitro electrophysiology, dynamic clamp, and modeling to characterize the interactions between a neuron’s intrinsic properties, the degree of gamma-band synchrony among its inhibitory inputs, and its spike timing. We apply these techniques to study six distinct types of cortical neurons. We find that neuron types systematically vary in the phase and precision of their spike timing relative to the peak of gamma frequency input, and the degree to which their spike time depended on changes in inhibitory synchrony. Biophysical characterizations of real neurons suggest that the membrane time constant (Tm), afterhyperpolarization amplitude and duration, and sodium channel properties are the key features governing gamma control of response timing. We confirmed these findings both in a single compartment model, and by using dynamic clamp to alter intrinsic features of neurons’ physiology. Shortening neurons’ time constant by adding artificial leak conductance enhanced neurons’ ability to entrain their firing and phase-precess, while adding an artificial afterhyperpolarization conductance reduced neurons’ ability to phase-precess. We conclude that a neuron’s intrinsic physiology substantially affects the ability of gamma-synchronized inhibitory inputs to control its response timing, and that different excitatory and inhibitory neuron types systematically differ in this regard. These results suggest that the characteristic phase relationship of the discharges of neurons during gamma activity may be explained by differences in intrinsic properties rather than differences in connectivity. Further, we note that the relevant physiology is not static, but may be altered by contextual or neuromodulatory factors; for instance, a neuron’s time constant decreases during intense synaptic activity, while its afterhyperpolarization is altered by neuromodulators such as noradrenaline and acetylcholine. We therefore suggest that the ability of gamma oscillations to control response timing is not fixed, but may be dynamically shaped to suit the cortex’s computational requirements during attention or cognition.
Conference:
Computational and Systems Neuroscience 2010, Salt Lake City, UT, United States, 25 Feb - 2 Mar, 2010.
Presentation Type:
Oral Presentation
Topic:
Oral presentations
Citation:
Hasenstaub
A,
Otte
S and
Callaway
EM
(2010). Neuronal biophysics modulate the ability of gamma oscillations to control
response timing..
Front. Neurosci.
Conference Abstract:
Computational and Systems Neuroscience 2010.
doi: 10.3389/conf.fnins.2010.03.00004
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Received:
17 Feb 2010;
Published Online:
17 Feb 2010.
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Correspondence:
Andrea Hasenstaub, Salk Institute for Biological Studies, Crick-Jacobs Center, La Jolla, United States, andrea.hasenstaub@gmail.com