title: A model of order-selectivity based on dynamic changes in the balance of excitation and inhibition produced by short-term synaptic plasticity.
abstract: Determining the order of sensory events separated by a few hundred milliseconds is critical to many forms of sensory processing, including vocalization and speech discrimination. Although many experimental studies have recorded from auditory order-sensitive and order-selective neurons, the underlying mechanisms are poorly understood. Here we demonstrate that universal properties of cortical synapses-short-term synaptic plasticity of excitatory and inhibitory synapses-are well suited for the generation of order-selective neural responses. Using computational models of canonical disynaptic circuits, we show that the dynamic changes in the balance of excitation and inhibition imposed by short-term plasticity lead to the generation of order-selective responses. Parametric analyses predict that among the forms of short-term plasticity expressed at excitatory-to-excitatory, excitatory-to-inhibitory, and inhibitory-to-excitatory synapses, the single most important contributor to order-selectivity is the paired-pulse depression of inhibitory postsynaptic potentials (IPSPs). A topographic model of the auditory cortex that incorporates short-term plasticity accounts for both context-dependent suppression and enhancement in response to paired tones. Together these results provide a framework to account for an important computational problem based on ubiquitous synaptic properties that did not yet have a clearly established computational function. Additionally, these studies suggest that disynaptic circuits represent a fundamental computational unit that is capable of processing both spatial and temporal information.
authors.affiliation: Integrative Center for Learning and Memory, Departments of Neurobiology and Psychology, UCLA, Los Angeles, California.
authors.forename: Vishwa
authors.initials: V
authors.lastname: Goudar
authors.affiliation: Integrative Center for Learning and Memory, Departments of Neurobiology and Psychology, UCLA, Los Angeles, California dbuono@ucla.edu.
authors.forename: Dean V
authors.initials: DV
authors.lastname: Buonomano
mesh_terms: D000200:Action Potentials / Q000502:physiology; D001303:Auditory Cortex / Q000502:physiology*; D001307:Auditory Perception / Q000502:physiology*; D003198:Computer Simulation; D053444:Inhibitory Postsynaptic Potentials / Q000502:physiology; D008959:Models, Neurological; D009433:Neural Inhibition / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000502:physiology; D017711:Nonlinear Dynamics; D013569:Synapses / Q000502:physiology; D009435:Synaptic Transmission / Q000502:physiology*; D018350:alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid / Q000378:metabolism; D005680:gamma-Aminobutyric Acid / Q000378:metabolism
chemical_list: D005680:gamma-Aminobutyric Acid; D018350:alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid
keywords: context-dependent suppression and enhancement; disynaptic circuit; order-selectivity; short-term synaptic plasticity