Synaptic regulation of spike firing in interneurons of the striatum in vivo
-
1
University of Bern, Department of Physiology, Switzerland
-
2
University of Otago, Department of Anatomy, Brain Health Research Centre, New Zealand
The striatum, the major input nucleus of the basal ganglia, is numerically dominated by a single class of principal neurons, the GABAergic spiny projection neuron (SPN) that has been extensively studied both in vitro and in vivo. Much less is known about the sparsely distributed interneurons, principally the cholinergic interneuron (CIN) and the GABAergic fast-spiking interneuron (FSI). Here, we summarize results from two recent studies on these interneurons where we used in vivo intracellular recording techniques in urethane-anaesthetized rats (Schulz et al., J Neurosci 31[31], 2011; J Physiol, in press). Interneurons were identified by their characteristic responses to intracellular current steps and spike waveforms. Spontaneous spiking contained a high proportion (~45%) of short inter-spike intervals (ISI) of <30 ms in FSIs, but virtually none in CINs. Spiking patterns in CINs covered a broad spectrum ranging from regular tonic spiking to phasic activity despite very similar unimodal membrane potential distributions across neurons. In general, phasic spiking activity occurred in phase with the slow ECoG waves, whereas CINs exhibiting tonic regular spiking were little affected by afferent network activity. In contrast, FSIs exhibited transitions between Down and Up states very similar to SPNs. Compared to SPNs, the FSI Up state membrane potential was noisier and power spectra exhibited significantly larger power at frequencies in the gamma range (55-95 Hz). Cortical-evoked inputs had faster dynamics in FSIs than SPNs and the membrane potential preceding spontaneous spike discharge exhibited short and steep trajectories, suggesting that fast input components controlled spike output in FSIs. Intrinsic resonance mechanisms may have further enhanced the sensitivity of FSIs to fast oscillatory inputs. Induction of an activated ECoG state by local ejection of bicuculline into the superior colliculus, resulted in increased spike frequency in both interneuron classes without changing the overall distribution of ISIs. This manipulation also made CINs responsive to a light flashed into the contralateral eye. Typically, the response consisted of an excitation at short latency followed by a pause in spike firing, via an underlying depolarization-hyperpolarization membrane sequence. These results highlight the differential sensitivity of striatal interneurons to afferent synaptic signals and support a model where CINs modulate the striatal network in response to salient sensory bottom-up signals, while FSIs serve gating of top-down signals from the cortex during action selection and reward-related learning.
Acknowledgements
This work was supported by The Marsden Fund of the Royal Society of New Zealand and the Neurological Foundation of New Zealand.
References
Schulz, J. M., Oswald M. J., and Reynolds, J. N. J. (2011). Visual-induced excitation leads to firing pauses in striatal cholinergic interneurons. J. Neurosci. 31, 11133–11143.
Schulz J. M., Pitcher T. L., Savanthrapadian S., Wickens J. R., Oswald M. J., Reynolds J. N. J. Enhanced high-frequency membrane potential fluctuations control spike output in striatal fast-spiking interneurones in vivo. J. Physiol. (Lond.) in press
Keywords:
cholinergic interneuron,
fast-spiking interneuron,
in vivo,
intracellular,
Striatum,
tonically active neuron,
Up state,
Urethane
Conference:
BC11 : Computational Neuroscience & Neurotechnology Bernstein Conference & Neurex Annual Meeting 2011, Freiburg, Germany, 4 Oct - 6 Oct, 2011.
Presentation Type:
Poster
Topic:
neurons, networks and dynamical systems (please use "neurons, networks and dynamical systems" as keywords)
Citation:
Schulz
JM and
Reynolds
JN
(2011). Synaptic regulation of spike firing in interneurons of the striatum in vivo.
Front. Comput. Neurosci.
Conference Abstract:
BC11 : Computational Neuroscience & Neurotechnology Bernstein Conference & Neurex Annual Meeting 2011.
doi: 10.3389/conf.fncom.2011.53.00176
Copyright:
The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers.
They are made available through the Frontiers publishing platform as a service to conference organizers and presenters.
The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated.
Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed.
For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions.
Received:
22 Aug 2011;
Published Online:
04 Oct 2011.
*
Correspondence:
Dr. Jan M Schulz, University of Bern, Department of Physiology, Bern, 3012, Switzerland, j.schulz@unibas.ch