Activation of the Cholinergic System Endows Compositional Properties to Striatal Cell Assemblies

Carillo-Reid L, Tecuapetla F, Ibanez-Sandoval O, Hernandez-Cruz A, Galarraga E, Bargas J. Activation of the cholinergic system endows compositional properties to striatal cell assemblies. J Neurophysiol 101: 737-749, 2009. First published November 19, 2008; doi:10.1152/jn.90975.2008. Striatal cell assemblies are thought to encode network states related to associative learning, procedural memory, and the sequential organization of behavior. Cholinergic neurotransmission modulates memory processes in the striatum and other brain structures. This work asks if the activity of striatal microcircuits observed in living nervous tissue, with attributes similar to cell assemblies, exhibit some of the properties proposed to be necessary to compose memory traces. Accordingly, we used whole cell and calcium-imaging techniques to investigate the cholinergic modulation of striatal neuron pools that have been reported to exhibit several properties expected from cell assemblies such as synchronous states of activity and the alternation of this activity among different neuron pools. We analyzed the cholinergic modulation of the activity of neuron pools with multidimensional reduction techniques and vectorization of network dynamics. It was found that the activation of the cholinergic system enables striatal cell assemblies with properties that have been posited for recurrent neural artificial networks with memory storage capabilities. Graph theory techniques applied to striatal network states revealed sequences of vectors with a recursive dynamics similar to closed reverberating cycles. The cycles exhibited a modular architecture and a hierarchical organization. It is then concluded that, under certain conditions, the cholinergic system enables the striatal microcircuit with the ability to compose complex sequences of activity. Neuronal recurrent networks with the characteristics encountered in the present experiments are proposed to allow repeated sequences of activity to become memories and repeated memories to compose learned motor procedures.