Detection of submillisecond spike timing differences based on delay-line anticoincidence detection

Abstract

Lyons-Warren AM, Kohashi T, Mennerick S, Carlson BA. Detection of submillisecond spike timing differences based on delayline anticoincidence detection. J Neurophysiol 110: 2295-2311. First published August 21, 2013 doi:10.1152/jn.00444.2013.-Detection of submillisecond interaural timing differences is the basis for sound localization in reptiles, birds, and mammals. Although comparative studies reveal that different neural circuits underlie this ability, they also highlight common solutions to an inherent challenge: processing information on timescales shorter than an action potential. Discrimination of small timing differences is also important for species recognition during communication among mormyrid electric fishes. These fishes generate a species-specific electric organ discharge (EOD) that is encoded into submillisecond-to-millisecond timing differences between receptors. Small, adendritic neurons (small cells) in the midbrain are thought to analyze EOD waveform by comparing these differences in spike timing, but direct recordings from small cells have been technically challenging. In the present study we use a fluorescent labeling technique to obtain visually guided extracellular recordings from individual small cell axons. We demonstrate that small cells receive 1-2 excitatory inputs from 1 or more receptive fields with latencies that vary by over 10 ms. This wide range of excitatory latencies is likely due to axonal delay lines, as suggested by a previous anatomic study. We also show that inhibition of small cells from a calyx synapse shapes stimulus responses in two ways: through tonic inhibition that reduces spontaneous activity and through precisely timed, stimulus-driven, feed-forward inhibition. Our results reveal a novel delay-line anticoincidence detection mechanism for processing submillisecond timing differences, in which excitatory delay lines and precisely timed inhibition convert a temporal code into a population code. temporal coding; electric fish; calyx; sound localization; interaural time difference TEMPORAL CODING, in which information is encoded into the precise timing of action potentials, is common in sensory systems ( VanRullen et al. 2005). In some cases, behavioral sensitivity can reach the submillisecond or even submicrosecond range, several orders of magnitude shorter than a typical action potential

Retrograde Fluorescent Labeling Allows for Targeted Extracellular Single-unit Recording from Identified Neurons <em>In vivo</em>

“…Successful recordings from labeled axons allow analysis of single-unit responses to sensory stimulation 18 . Figure 5A shows representative action potentials evoked by transverse electrosensory stimulation using bipolar electrodes located on the insides of the left and right walls of the recording chamber.…”

Genetic drift does not sufficiently explain patterns of electric signal variation among populations of the mormyrid electric fishParamormyrops kingsleyae

“…Our field and laboratory results together highlight that there is considerable variation between individuals (Fig 9A) in the ability to discriminate between EOD waveforms, suggesting that some individuals may be more capable than others at performing the dishabituation task. Based on several studies that have characterized the neural encoding of EOD waveforms (Amagai et al 1998;Friedman and Hopkins 1998;Xu-Friedman and Hopkins 1999;Carlson 2009;Baker et al 2013;Lyons-Warren et al 2013), we originally predicted that P.…”

“…This suggests that neural 'innovation' may, at least at macroevolutionary scales, facilitate EOD divergence. Detailed physiological and behavioral data implicate these changes lead to increased ability to discriminate finescale differences in EOD waveforms Lyons-Warren et al 2013). …”

Sensory Specializations of Mormyrid Fish Are Associated with Species Differences in Electric Signal Localization Behavior

“…This means that knollenorgans on one side of the body respond to rising edges of a stimulus, while knollenorgans on the opposite side of the body respond to falling edges [Bennett, 1965]. Spike timing differences among electroreceptors on opposite sides of the body encode signal duration and waveform, and may provide information about sender location [Friedman and Hopkins, 1998;Lyons-Warren et al, 2013a].…”

“…The midbrain exterolateral nucleus (EL), a brain region devoted to processing communication signals [Bennett and Steinbach, 1969;Bell and Grant, 1989;Amagai, 1998;Vélez and Carlson, 2016], is enlarged and subdivided into anterior (ELa) and posterior (ELp) regions in species that have distributed electroreceptors and are sensitive to EOD waveform variation [Carlson et al, 2011]. In these species, EOD sensitivity arises in ELa and is achieved by comparing spike timing differences among electroreceptors on opposite sides of the body in an excitatory-inhibitory circuit [Friedman and Hopkins, 1998;Lyons-Warren et al, 2013a]. In contrast, EL is small and undifferentiated in species with clustered electroreceptors that are insensitive to EOD waveform variation [Carlson et al, 2011].…”