Abstract

Oscillations are ubiquitous features of neuronal activity in sensory systems and are considered as a substrate for the integration of sensory information. Several studies have described oscillatory activity in the geniculate visual pathway, but little is known about this phenomenon in the extrageniculate visual pathway. We describe oscillations in evoked and background activity in the cat's superficial layers of the superior colliculus, a retinorecipient structure in the extrageniculate visual pathway. Extracellular single-unit activity was recorded during periods with and without visual stimulation under isoflurane anesthesia in the mixture of N2O/O2. Autocorrelation, FFT and renewal density analyses were used to detect and characterize oscillations in the neuronal activity. Oscillations were common in the background and stimulus-evoked activity. Frequency range of background oscillations spanned between 5 and 90 Hz. Oscillations in evoked activity were observed in about half of the cells and could appear in two forms —stimulus-phase-locked (10–100 Hz), and stimulus-phase-independent (8–100 Hz) oscillations. Stimulus-phase-independent and background oscillatory frequencies were very similar within activity of particular neurons suggesting that stimulus-phase-independent oscillations may be a form of enhanced “spontaneous” oscillations. Stimulus-phase-locked oscillations were present in responses to moving and flashing stimuli. In contrast to stimulus-phase-independent oscillations, the strength of stimulus-phase-locked oscillations was positively correlated with stimulus velocity and neuronal firing rate. Our results suggest that in the superficial layers of the superior colliculus stimulus-phase-independent oscillations may be generated by the same mechanism(s) that lie in the base of “spontaneous” oscillations, while stimulus-phase-locked oscillations may result from interactions within the intra-collicular network and/or from a phase reset of oscillations present in the background activity.

Highlights

  • Information about the external world is transferred to the brain via trains of action potentials that can exhibit a repetitive temporal structure

  • Stimulus-phase-locked oscillations were revealed by (1) the presence of apparent changes in the firing rate during and/or shortly after visual stimulation, that were clearly visible in the form of vertical stripes in the raster plots and as a specific temporal pattern in averaged Peri-stimulus time histograms (PSTHs), (2) the presence of a second oscillatory peak in the ACHPSTH computed from averaged PSTHs, as well as (3) the presence of a prominent peak (z-score > 2) in the computed from ACHPSTH power spectrum

  • Stimulus-phase-independent oscillations were identified by (1) the presence of a second oscillatory peak in the Raw autocorrelation histograms (rACHs) computed from a spike train obtained for each single stimulus repetition and averaged over number of repetitions, and corrected by subtraction of the stimulus-dependent shift predictor, and (2) the presence of a prominent peak (z-score > 2) in the power spectrum computed from cACH

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Summary

Introduction

Information about the external world is transferred to the brain via trains of action potentials that can exhibit a repetitive temporal structure. These temporal patterns, formed by the periodic appearance of single spikes, bursts of spikes, or periodic changes in the firing rate are called oscillations (Lestienne, 2001). The main visual input to sSC originates in the retina (Hoffmann, 1972; Graybiel, 1974, 1975; for review see Waleszczyk et al, 2004; May, 2006), but the sSC are the target of descending projections from multiple visual cortices (Harting et al, 1992)

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