Cell-type-specific resonances shape the responses of striatal neurons to synaptic input

Abstract

Beatty JA, Song SC, Wilson CJ. Cell-type-specific resonances shape the responses of striatal neurons to synaptic input. J Neurophysiol 113: 688 -700, 2015. First published November 19, 2014 doi:10.1152/jn.00827.2014.-Neurons respond to synaptic inputs in cell-type-specific ways. Each neuron type may thus respond uniquely to shared patterns of synaptic input. We applied statistically identical barrages of artificial synaptic inputs to four striatal cell types to assess differences in their responses to a realistic input pattern. Each interneuron type fired in phase with a specific input-frequency component. The fast-spiking interneuron fired in relation to the gamma-band (and higher) frequencies, the low-threshold spike interneuron to the beta-band frequencies, and the cholinergic neurons to the delta-band frequencies. Low-threshold spiking and cholinergic interneurons showed input impedance resonances at frequencies matching their spiking resonances. Fast-spiking interneurons showed resonance of input impedance but at lower than gamma frequencies. The spiny projection neuron's frequency preference did not have a fixed frequency but instead tracked its own firing rate. Spiny cells showed no input impedance resonance. Striatal interneurons are each tuned to a specific frequency band corresponding to the major frequency components of local field potentials. Their influence in the circuit may fluctuate along with the contribution of that frequency band to the input. In contrast, spiny neurons may tune to any of the frequency bands by a change in firing rate.

Pyramidal Cell-Interneuron Circuit Architecture and Dynamics in Hippocampal Networks

“…This included examples of connections which had ‘preferred’ interspike intervals, some correlating to the resonant properties of some interneurons as well as the timescales of hippocampal population rhythms. The role of postsynaptic resonance is supported by our finding that transmission probability is highest for specific postsynaptic ISI’s (Figure 7), which are in the temporal range of spiking resonance observed in interneurons recorded in vitro (Beatty et al, 2015, Pike et al, 2000). Overall, our findings indicate that short-term plasticity is synapse-specific rather than neuron-specific, and that frequency filtering of spike transmission can be exploited for tuning network dynamics.…”

Resonant Interneurons Can Increase Robustness of Gamma Oscillations

“…For all experimental protocols, synaptic conductances were simulated using dynamic clamp software (Dorval et al, 2001;Bettencourt et al, 2008;Lin et al, 2010) on a Pentium 4 computer running Linux Ubuntu with a patched version of the real-time application interface (RTAI) kernel. Voltage was measured and a control current applied with a MultiClamp 700B amplifier (Molecular Devices…”

“…There is another excitability type in which neurons are instead resonators with a cutoff frequency below which they cannot fire. We call this type of resonance "spiking resonance" (Beatty et al, 2015) to avoid confusion with the "subthreshold resonance" (Hutcheon and Yarom, 2000) that is often measured using a ZAP signal. There is strong evidence that the parvalbumin-containing, fast-spiking (FS) basket cells are critical for gamma rhythmogenesis both in vitro (Gulyás et al, 2010) and in vivo (Cardin et al, 2009).…”

Prolonged withdrawal from cocaine self‐administration affects prefrontal cortex‐ and basolateral amygdala–nucleus accumbens core circuits but not accumbens GABAergic local interneurons

“…Different types of striatal interneurons are preferentially engaged by different patterns of cortical stimulation (Beatty et al, 2015); therefore, an alteration at a specific frequency may suggest an alteration of a specific group of neurons. For example, in striatum, PV+ interneurons generate action potentials primarily at input frequencies in the gamma range, so a difference between groups when train stimulations are conducted at 40 Hz may be suggestive of altered activity of PV+ interneurons; changes in the delta range (1–5 Hz) and beta range (10–30 Hz) may indicate effects on cholinergic and LTS interneurons, respectively (Beatty et al, 2015; Jayasinghe et al, 2015). …”