Dynamics of Stimulus-Evoked Spike Timing Correlations in the Cat Lateral Geniculate Nucleus

Abstract

Precisely synchronized neuronal activity has been commonly observed in the mammalian visual pathway. Spike timing correlations in the lateral geniculate nucleus (LGN) often take the form of phase synchronized oscillations in the high gamma frequency range. To study the relations between oscillatory activity, synchrony, and their time-dependent properties, we recorded activity from multiple single units in the cat LGN under stimulation by stationary spots of light. Autocorrelation analysis showed that approximately one third of the cells exhibited oscillatory firing with a mean frequency ϳ80 Hz. Cross-correlation analysis showed that 30% of unit pairs showed significant synchronization, and 61% of these pairs consisted of synchronous oscillations. Crosscorrelation analysis assumes that synchronous firing is stationary and maintained throughout the period of stimulation. We tested this assumption by applying unitary events analysis (UEA). We found that UEA was more sensitive to weak and transient synchrony than cross-correlation analysis and detected a higher incidence (49% of cell pairs) of significant synchrony (unitary events). In many unit pairs, the unitary events were optimally characterized at a bin width of 1 ms, indicating that neural synchrony has a high degree of temporal precision. We also found that approximately one half of the unit pairs showed nonstationary changes in synchrony that could not be predicted by the modulation of firing rates. Population statistics showed that the onset of synchrony between LGN cells occurred significantly later than that observed between retinal afferents and LGN cells. The synchrony detected among unit pairs recorded on separate tetrodes tended to be more transient and have a later onset than that observed between adjacent units. These findings show that stimulus-evoked synchronous activity within the LGN is often rhythmic, highly nonstationary, and modulated by endogenous processes that are not tightly correlated with firing rate. I N T R O D U C T I O NSynchronous activity is a widespread and robust property of neuronal networks in a wide variety of species (Buzsáki 2006;Laurent et al. 2001;Singer and Gray 1995;Usrey and Reid 1999). Its functional significance has long been recognized within the context of synaptic physiology, where it plays a critical role in synaptic integration and plasticity (Alonso et al. 1996;Azouz and Gray 2003;Toyama et al. 1981;Usrey and Reid 1999). In recent years, synchronous activity on a millisecond time scale has been postulated to contribute to higherlevel functions including perceptual grouping (Gray 1999; (HerculanoHouzel et al. 1999). In each of these contexts, it has been argued that temporally correlated activity should be highly dynamic to provide representational flexibility (Engel et al. 2001;Fries 2005;Fujii et al. 1996;Gerstein et al. 1989;Gray 1999;Gruen et al. 2003;Samonds et al. 2006;Singer 1994; Von der Malsburg 1981).Such dynamic changes in correlated activity could result from stimulus or task driven influences or b...

Gamma and infra‐slow oscillations shape neuronal firing in the rat subcortical visual system

“…In cat LGN, high gamma oscillatory activity was found irrespective of receptive field properties or laminar position (Ito et al . ), which is similar to the present study showing that the expression of a HDP was not confined to any particular type of visual response.…”

“…; Ito et al . ), although it is tempting to speculate that the HDP in the LGN and OPN share the same origin as that reported in the SCN (Tsuji et al . ) because they have similar characteristics.…”

“…This functional hypothesis was strengthened by the results of a recent study in mice showing that retinal gamma encodes information critical for global object recognition (Ito et al . ), which also comprises relevant information for non‐image forming functions and reflexes.…”

“…; Neuenschwander & Singer, ; Ito et al . ). Furthermore, multimodal ISI histograms are proposed to be a feature of sensory systems and were also found in shark thermoreceptor cells (Braun et al .…”

State-Space Analysis of Time-Varying Higher-Order Spike Correlation for Multiple Neural Spike Train Data

“…Assembly activity was hypothesized to organize dynamically as a result of sensory input and/or in relation to behavioral context [6]–[10]. Supportive experimental evidence was provided by findings of the presence of excess spike synchrony occurring dynamically in relation to stimuli [11]–[14], behavior [14]–[19], or internal states such as memory retention, expectation, and attention [8], [20]–[23].…”