Temporal Convergence of Dynamic Cell Assemblies in the Striato-Pallidal Network

Abstract

The basal ganglia (BG) have been hypothesized to implement a reinforcement learning algorithm. However, it is not clear how information is processed along this network, thus enabling it to perform its functional role. Here we present three different encoding schemes of visual cues associated with rewarding, neutral, and aversive outcomes by BG neuronal populations.We studied the response profile and dynamical behavior of two populations of projection neurons [striatal medium spiny neurons (MSNs), and neurons in the external segment of the globus pallidus (GPe)], and one neuromodulator group [striatal tonically active neurons (TANs)] from behaving monkeys. MSNs and GPe neurons displayed sustained average activity to cue presentation. The population average response of MSNs was composed of three distinct response groups that were temporally differentiated and fired in serial episodes along the trial. In the GPe, the average sustained response was composed of two response groups that were primarily differentiated by their immediate change in firing rate direction. However, unlike MSNs, neurons in both GPe response groups displayed prolonged and temporally overlapping persistent activity. The putamen TANs stereotyped response was characterized by a single transient response group. Finally, the MSN and GPe response groups reorganized at the outcome epoch, as different task events were reflected in different response groups.Our results strengthen the functional separation between BG neuromodulators and main axis neurons. Furthermore, they reveal dynamically changing cell assemblies in the striatal network of behaving primates. Finally, they support the functional convergence of the MSN response groups onto GPe cells.

Dopamine regulates distinctively the activity patterns of striatal output neurons in advanced parkinsonian primates

“…The prominent burst activity of MSNs found at the baseline parkinsonian state at rest clearly contrasts with their phasic, single-spike firing at very low frequency (0 -2 Hz) observed in normal animals (Adler et al 2012(Adler et al , 2013Barnes et al 2005;Crutcher and DeLong 1984a;Kimura 1992). As described in other basal ganglia regions (Filion and Tremblay 1991;Heimer et al 2002;Raz et al 2000), this bursting pattern may be caused by DA loss.…”

Parallel Processing of Environmental Recognition and Locomotion in the Mouse Striatum

“…The dynamic formation of MSN cell assemblies comprising functional reorganization into different response groups at different trial epochs has been described previously (Adler et al, 2012). In that study, MSNs belonging to different response clusters were differentiated primarily by their temporal profile and not their anatomical or neurochemical properties.…”

“…The properties of three of the clusters fit those of the MSNs, FSI, and TANs; nonetheless, their sampling probabilities were not representative of the anatomy, thus raising a concern regarding their identification. However, studies that previously identified these neurons in primates (Kimura, 1990;Adler et al, 2012) and in rodents Gage et al, 2010;Yarom and Cohen, 2011) report different sampling biases, suggesting that despite the bias the neurons' identification remains valid.…”

Encoding by Synchronization in the Primate Striatum

“…The Hebrew University is an Association for Assessment and Accreditation of Laboratory Animal Care internationally accredited institution. Surgery procedures, datarecording methods, and single cell analysis have been described in detail previously (Adler et al, 2010;Adler et al, 2012). We present them briefly here and describe the methods not used in the previous manuscripts.…”

“…We conducted a clustering analysis to differentiate the activity of single medium spiny neurons (MSNs) into groups of cells with similar response profiles (Adler et al, 2012). Briefly, we first characterized the neural responses to the behavioral events by the poststimulus time histogram (PSTH) and then ran a principal component analysis on the normalized PSTHs.…”