title: Emerging feed-forward inhibition allows the robust formation of direction selectivity in the developing ferret visual cortex.
abstract: The computation of direction selectivity requires that a cell respond to joint spatial and temporal characteristics of the stimulus that cannot be separated into independent components. Direction selectivity in ferret visual cortex is not present at the time of eye opening but instead develops in the days and weeks following eye opening in a process that requires visual experience with moving stimuli. Classic Hebbian or spike timing-dependent modification of excitatory feed-forward synaptic inputs is unable to produce direction-selective cells from unselective or weakly directionally biased initial conditions because inputs eventually grow so strong that they can independently drive cortical neurons, violating the joint spatial-temporal activation requirement. Furthermore, without some form of synaptic competition, cells cannot develop direction selectivity in response to training with bidirectional stimulation, as cells in ferret visual cortex do. We show that imposing a maximum lateral geniculate nucleus (LGN)-to-cortex synaptic weight allows neurons to develop direction-selective responses that maintain the requirement for joint spatial and temporal activation. We demonstrate that a novel form of inhibitory plasticity, postsynaptic activity-dependent long-term potentiation of inhibition (POSD-LTPi), which operates in the developing cortex at the time of eye opening, can provide synaptic competition and enables robust development of direction-selective receptive fields with unidirectional or bidirectional stimulation. We propose a general model of the development of spatiotemporal receptive fields that consists of two phases: an experience-independent establishment of initial biases, followed by an experience-dependent amplification or modification of these biases via correlation-based plasticity of excitatory inputs that compete against gradually increasing feed-forward inhibition.
authors.affiliation: Department of Biology, Brandeis University, Waltham, Massachusetts; Sloan-Swartz Center for Theoretical Neurobiology, Brandeis University, Waltham, Massachusetts; Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts; vanhooser@brandeis.edu.
authors.forename: Stephen D
authors.initials: SD
authors.lastname: Van Hooser
authors.affiliation: Department of Biology, Brandeis University, Waltham, Massachusetts; Sloan-Swartz Center for Theoretical Neurobiology, Brandeis University, Waltham, Massachusetts; Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts;
authors.forename: Gina M
authors.initials: GM
authors.lastname: Escobar
authors.affiliation: Department of Neurobiology and Behavior, State University of New York-Stony Brook, Stony Brook, New York; and SUNY Eye Institute, State University of New York-Stony Brook, Stony Brook, New York.
authors.forename: Arianna
authors.initials: A
authors.lastname: Maffei
authors.affiliation: Department of Biology, Brandeis University, Waltham, Massachusetts; Sloan-Swartz Center for Theoretical Neurobiology, Brandeis University, Waltham, Massachusetts; Volen Center for Complex Systems, Brandeis University, Waltham, Massachusetts;
authors.forename: Paul
authors.initials: P
authors.lastname: Miller
mesh_terms: D000222:Adaptation, Physiological / Q000502:physiology; D000818:Animals; D003198:Computer Simulation; D025461:Feedback, Physiological / Q000502:physiology*; D005289:Ferrets; D005829:Geniculate Bodies / Q000502:physiology; D008959:Models, Neurological; D009039:Motion Perception / Q000502:physiology*; D009415:Nerve Net / Q000502:physiology*; D009433:Neural Inhibition / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology; D014793:Visual Cortex / Q000254:growth & development* / Q000502:physiology*; D014794:Visual Fields / Q000502:physiology
keywords: Hebbian learning; Reichardt detector; feed-forward; logical AND-gate; unsupervised learning