Circuit dynamics of the superior colliculus revealed by in vitro voltage imaging

Department of Neuroscience, School of Medicine and Public Health, University of Wisconsin, Madison, Wisconsin 53706, USA.
Annals of the New York Academy of Sciences (Impact Factor: 4.38). 09/2011; 1233(1):41-7. DOI: 10.1111/j.1749-6632.2011.06166.x
Source: PubMed


The superior colliculus (SC) is well known for its involvement in the conversion of sensory stimuli into motor commands. This sensorimotor integration is made possible by the collective activity of multiple neuronal connections throughout the SC. Still, the majority of SC research focuses on in vivo extracellular recordings of behaving monkeys or in vitro patch-clamp recordings from lower mammals. Here, we discuss the results of an in vitro voltage-imaging technique in which population activity across the rodent SC circuitry was visualized to bridge the gap between single-cell recordings and whole-animal behavior. The high temporal and spatial resolution of the voltage-imaging technique allowed us to visualize patterns of activity following stimulation at discrete laminae. Stimulation within either the superficial or intermediate layer showed recruitment of disparate SC circuitry. These results provide insight into the circuit dynamics and neuronal populations that underlie behavior.

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Available from: Michele A Basso, Jun 12, 2014
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    ABSTRACT: The superior colliculus (SC) is critical in localizing salient visual stimuli and making decisions on the location of the next saccade. Lateral interactions across the spatial map of the SC are hypothesized to help mediate these processes. Here, we investigate lateral interactions within the SC by applying whole-cell recordings in horizontal slices of mouse SC, which maintained the local structure of the superficial (SCs) visual layer, which is hypothesized to participate in localizing salient stimuli, and the intermediate (SCi) layer, which is supposed to participate in saccade decision-making. When effects of either electrical or chemical (uncaging of free glutamate) stimuli were applied to multiple sites with various distances from the recorded cell, a pattern of center excitation-surround inhibition was found to be prominent in SCs. When the interactions of synaptic effects induced by simultaneous stimulation of two sites were tested, non-linear facilitatory or inhibitory interactions were observed. In contrast, in the SCi, stimulation induced mainly excitation, which masked underlying inhibition. The excitatory synaptic effects of stimulation applied at remote sites were summed in a near linear manner. The result suggested that SCs lateral interactions appear suitable for localizing salient stimuli, while the lateral interactions within SCi are more suitable for faithfully accumulating subthreshold signals for saccadic decision-making. Implementation of this laminar-specific organization makes the SC a unique structure for serially processing signals for saliency localization and saccadic decision-making.
    European Journal of Neuroscience 04/2014; 40(2). DOI:10.1111/ejn.12579 · 3.18 Impact Factor