Abstract
Spike trains from neurons in the basal ganglia of parkinsonian primates show increased pairwise correlations, oscillatory activity, and burst rate compared to those from neurons recorded during normal brain activity. However, it is not known how these changes affect the behavior of downstream thalamic neurons. To understand how patterns of basal ganglia population activity may affect thalamic spike statistics, we study pairs of model thalamocortical (TC) relay neurons receiving correlated inhibitory input from the internal segment of the globus pallidus (GPi), a primary output nucleus of the basal ganglia. We observe that the strength of correlations of TC neuron spike trains increases with the GPi correlation level, and bursty firing patterns such as those seen in the parkinsonian GPi allow for stronger transfer of correlations than do firing patterns found under normal conditions. We also show that the T-current in the TC neurons does not significantly affect correlation transfer, despite its pronounced effects on spiking. Oscillatory firing patterns in GPi are shown to affect the timescale at which correlations are best transferred through the system. To explain this last result, we analytically compute the spike count correlation coefficient for oscillatory cases in a reduced point process model. Our analysis indicates that the dependence of the timescale of correlation transfer is robust to different levels of input spike and rate correlations and arises due to differences in instantaneous spike correlations, even when the long timescale rhythmic modulations of neurons are identical. Overall, these results show that parkinsonian firing patterns in GPi do affect the transfer of correlations to the thalamus.
Highlights
Much research has been dedicated to the study of how parkinsonian conditions affect the firing patterns of the basal ganglia
By imposing high frequency rhythms, deep brain stimulation (DBS) could decrease the thalamic sensitivity to changes in input correlations that we find with globus pallidus (GPi) inputs in the 4–10 Hz range and that could be provoked by pathologically synchronized firing rate modulations in the basal ganlia in parkinsonism
In our study, we have predicted that firing patterns, such as oscillations and bursting, observed in the GPi under parkinsonian conditions directly affect the correlation present between GPi output signals as well as the way that correlations are transferred from GPi to thalamus
Summary
Much research has been dedicated to the study of how parkinsonian conditions affect the firing patterns of the basal ganglia. An increase in the rate of oscillatory bursts has been found in neurons in the globus pallidus (GPi) of monkeys treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP), which induces a parkinsonian state (Bergman et al, 1998; Wichmann et al, 1999; Wichmann and Soares, 2006). While little correlation is normally present in the activity of GPi neurons (Nini et al, 1995; Bar-Gad et al, 2003), significant correlations between the outputs of GPi neurons arise in non-human primates treated with MPTP (Nini et al, 1995; Bergman et al, 1998; Raz et al, 2000; Heimer et al, 2006) and in humans with Parkinson’s disease (Hurtado et al, 1999; Gale et al, 2008). While the implications of parkinsonian changes in single GPi neuron firing patterns have been considered theoretically, the effects of the temporal relationships emerging within GPi population activity have yet to be investigated computationally
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