Stimulus-Dependent Modulation of Spike Burst Length in Cat Striate Cortical Cells

Abstract

Burst activity, defined by groups of two or more spikes with intervals of < or = 8 ms, was analyzed in responses to drifting sinewave gratings elicited from striate cortical neurons in anesthetized cats. Bursting varied broadly across a population of 507 simple and complex cells. Half of this population had > or = 42% of their spikes contained in bursts. The fraction of spikes in bursts did not vary as a function of average firing rate and was stationary over time. Peaks in the interspike interval histograms were found at both 3-5 ms and 10-30 ms. In many cells the locations of these peaks were independent of firing rate, indicating a quantized control of firing behavior at two different time scales. The activity at the shorter time scale most likely results from intrinsic properties of the cell membrane, and that at the longer scale from recurrent network excitation. Burst frequency (bursts per s) and burst length (spikes per burst) both depended on firing rate. Burst frequency was essentially linear with firing rate, whereas burst length was a nonlinear function of firing rate and was also governed by stimulus orientation. At a given firing rate, burst length was greater for optimal orientations than for nonoptimal orientations. No organized orientation dependence was seen in bursts from lateral geniculate nucleus cells. Activation of cortical contrast gain control at low response amplitudes resulted in no burst length modulation, but burst shortening at optimal orientations was found in responses characterized by supersaturation. At a given firing rate, cortical burst length was shortened by microinjection of gamma-aminobutyric acid (GABA), and bursts became longer in the presence of N-methyl-bicuculline, a GABA(A) receptor blocker. These results are consistent with a model in which responses are reduced at nonoptimal orientations, at least in part, by burst shortening that is mediated by GABA. A similar mechanism contributes to response supersaturation at high contrasts via recruitment of inhibitory responses that are tuned to adjacent orientations. Burst length modulation can serve as a form of coding by supporting dynamic, stimulus-dependent reorganization of the effectiveness of individual network connections.

In vivo conditions influence the coding of stimulus features by bursts of action potentials

“…Indeed, a previous modeling study using a minimal model of a Hippocampal pyramidal neuron has shown burst duration coding in the form of a positive correlation between stimulus slope and burst length (Kepecs et al 2002). This is consistent with experimental results showing correlations between the burst length and stimulus attributes such as orientation (DeBusk et al 1997;Martinez-Conde et al 2002), velocity (Arganda et al 2007, luminance (Gaudry and Reinagel 2008), and sound (Eyherabide et al 2008;Marsat and Pollack 2010). While our modeling results and in vitro data also show a positive correlation between stimulus slope and burst length for ELL pyramidal neurons, our results suggest that the weak correlation between burst length and stimulus amplitude can be accounted by the high variability displayed by ELL neurons in vivo.…”

“…the temporal ordering of spikes within a burst or the number of spikes within a burst) and stimulus attributes (e.g. its amplitude of its rate of rise before burst onset), thereby suggesting that the detailed structure of a burst could provide information about the stimulus (DeBusk et al 1997;Kepecs et al 2002;Martinez-Conde et al 2002;Oswald et al 2007;Eyherabide et al 2008;Gaudry and Reinagel 2008;Marsat and Pollack 2010;Samengo and Montemurro 2010). Studies conducted in simple systems with well-characterized anatomy and relatively simple behaviors are likely to yield significant insight into the functional role of burst firing.…”

Chemosensory burst coding by mouse vomeronasal sensory neurons

“…Bursts have been reported to encode sensory information in numerous systems including in olfactory receptor neurons (Eyherabide et al 2008;Rospars et al 2000). In various brain regions, the utility of bursts has been attributed to encoding information by burst duration (Kepecs et al 2002;DeBusk et al 1997;Martinez-Conde et al 2002), number of spikes within the burst (Eyherabide et al 2008), or within-burst ISI (Oswald et al 2007).…”

Parallel Processing of Sensory Input by Bursts and Isolated Spikes

“…1 A2,B2), an ISI criterion was established to identify spikes belonging to bursts (Turner et al, 1994(Turner et al, , 1996Debusk et al, 1997;Metzner et al, 1998;Reinagel et al, 1999). A criterion ISI of 10 msec was chosen for in vitro data.…”