Encoding by Synchronization in the Primate Striatum

Abstract

Information is encoded in the nervous system through the discharge and synchronization of single neurons. The striatum, the input stage of the basal ganglia, is divided into three territories: the putamen, the caudate, and the ventral striatum, all of which converge onto the same motor pathway. This parallel organization suggests that there are multiple and competing systems in the basal ganglia network controlling behavior. To explore which mechanism(s) enables the different striatal domains to encode behavioral events and to control behavior, we compared the neural activity of phasically active neurons [medium spiny neurons (MSNs), presumed projection neurons] and tonically active neurons (presumed cholinergic interneurons) across striatal territories from monkeys during the performance of a well practiced task. Although neurons in all striatal territories displayed similar spontaneous discharge properties and similar temporal modulations of their discharge rates to the behavioral events, their correlation structure was profoundly different. The distributions of signal and noise correlation of pairs of putamen MSNs were strongly shifted toward positive correlations and these two measures were correlated. In contrast, MSN pairs in the caudate and ventral striatum displayed symmetrical, near-zero signal and noise correlation distributions. Furthermore, only putamen MSN pairs displayed different noise correlation dynamics to rewarding versus neutral/aversive cues. Similarly, the noise correlation between tonically active neuron pairs was stronger in the putamen than in the caudate. We suggest that the level of synchronization of the neuronal activity and its temporal dynamics differentiate the striatal territories and may thus account for the different roles that striatal domains play in behavioral control.

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.…”

Activity Dynamics and Signal Representation in a Striatal Network Model with Distance-Dependent Connectivity

“…Weak background inputs or high input variance induced unstructured AI activity, whereas stronger background inputs or low input variance induced stable dynamics (e.g., WTA). For moderately strong inputs, the network activity organized into unstable spatial bumps [transition activity (TA)] resembling the experimentally observed NAs (Adler et al, 2013; Barbera et al, 2016). Finally, we describe how stimulus response characteristics are affected by the ongoing activity state of the network.…”

“…Recent observations of temporal (Adler et al, 2013) and spatial (Barbera et al, 2016) clustering of spiking activity in the striatum suggest that striatal activity may be organized in transient coactivations of groups of neurons. Such coactivated neuron groups can be termed neuronal assemblies (NAs).…”

Searching for Conservation Laws in Brain Dynamics—BOLD Flux and Source Imaging

“…There, it has been argued that lssfMRI might be sensitive to spatial neuronal synchronization, specifically on spatial scales accessible to BOLD fMRI. A recent investigation of such spatial synchronization measured with electrodes in the striatum of macaques [77] might support this notion: These authors found a functional specialization of the putamen in the sense that pairs of putaminal medium spiny neurons were synchronized (by means of correlation) during a classical conditioning task. In contrast, neurons in the caudate and ventral striatum were not.…”