Globus Pallidus external segment neuron classification in freely moving rats: a comparison to primates

Abstract

Globus Pallidus external segment (GPe) neurons are well-characterized in behaving primates. Based on their firing properties, these neurons are commonly divided into two distinct groups: high frequency pausers (HFP) and low frequency bursters (LFB). However, no such characterization has been made for behaving rats. The current study characterizes and categorizes extracellularly recorded GPe neurons in freely moving rats, and compares these results to those obtained by extracellular recordings in behaving primates using the same analysis methods. Analysis of our data recorded in rats revealed two distinct neuronal populations exhibiting firing-pattern characteristics that are similar to those obtained in primates. These characteristic firing patterns are conserved between species although the firing rate is significantly lower in rats than in primates. Significant differences in waveform duration and shape were insufficient to create a reliable waveform-based classification in either species. The firing pattern analogy may emphasize conserved processing properties over firing rate per-se. Given the similarity in GPe neuronal activity between human and non-human primates in different pathologies, our results encourage information transfer using complementary studies across species in the GPe to acquire a better understanding of the function of this nucleus in health and disease.

Figure 1. Verification of electrode placement in the Globus Pallidus of rats.

A: a 60 micron slice showing electrode placement in a rat GPe following electrolytic lesion. B: Appropriate coronal section from atlas (Bregma: −2.28 mm; [47]). C: Recording sites marked (grey rectangle) for all animals on a planar rat atlas slice (Bregma: −6.82 mm; [47]).

Figure 2. Typical firing patterns observed in rats (A–C) and primates (D–F).

Left panel: autocorrelation using a time window of ±1 s, middle panel: autocorrelation with x-axis expanded to ±0.1 s, right panel: spike train of the example neuron. A: example of HFP neuron exhibiting tonic Poisson firing without pauses. B: HFP neuron displaying pauses (pauser). C: LFB neuron (burster). D–F: same type of neurons as in A–C but in primates.

Figure 3. Neuronal classification and firing properties in primates and rats.

A and B: 3 dimensional presentation of firing properties leading to the formation of distinct clusters in primates (A) and rats (B). C–H: Bar plots representing parameters of the two groups (HFP - blue, LFB - red) in the two species (left two bars - primates, right two bars - rats).

Figure 4. Waveform characteristics.

A and B: normalized average waveforms of HFP (blue) and LFB (red) neurons in primates (A) and rats (B). Inset: X represents the valley to peak duration, Y the valley width and Z the zero-cross parameter. C and D Bar plots representing waveform parameters in HFP (blue) and LFB (red) neurons in primates (C) and in rats (D).

Figure 5. GPe neurons exhibit negligible interactions between pairs of neurons.

Cross-correlations in the two species. Below the blue line: cross-correlations during a time window of ±1 s in four units recorded simultaneously in primates. Above the blue line: same in rats. Red lines in every cross-correlogram represent the lower and upper confidence levels (see Methods).