Person:

Kreiman, Gabriel

We investigated the variability of P-receptor afferent spike trains in the weakly electric fish, Eigenmannia, to repeated presentations of random electric field AMs (RAMs) and quantified its impact on the encoding of time-varying stimuli. A new measure of spike timing jitter was developed using the notion of spike train distances recently introduced by Victor and Purpura. This measure of variability is widely applicable to neuronal responses, irrespective of the type of stimuli used (deterministic vs. random) or the reliability of the recorded spike trains. In our data, the mean spike count and its variance measured in short time windows were poorly correlated with the reliability of P-receptor afferent spike trains, implying that such measures provide unreliable indices of trial-to-trial variability. P-receptor afferent spike trains were considerably less variable than those of Poisson model neurons. The average timing jitter of spikes lay within 1–2 cycles of the electric organ discharge (EOD). At low, but not at high firing rates, the timing jitter was dependent on the cutoff frequency of the stimulus and, to a lesser extent, on its contrast. When spikes were artificially manipulated to increase jitter, information conveyed by P-receptor afferents was degraded only for average jitters considerably larger than those observed experimentally. This suggests that the intrinsic variability of single spike trains lies outside of the range where it might degrade the information conveyed, yet still allows for improvement in coding by averaging across multiple afferent fibers. Our results were summarized in a phenomenological model of P-receptor afferents, incorporating both their linear transfer properties and the variability of their spike trains. This model complements an earlier one proposed by Nelson et al. for P-receptor afferents of Apteronotus. Because of their relatively high precision with respect to the EOD cycle frequency, P-receptor afferent spike trains possess the temporal resolution necessary to support coincidence detection operations at the next stage in the amplitude-coding pathway.

Neighboring cells in topographical sensory maps may transmit similar information to the next higher level of processing. How information transmission by groups of nearby neurons compares with the performance of single cells is a very important question for understanding the functioning of the nervous system. To tackle this problem, we quantified stimulus-encoding and feature extraction performance by pairs of simultaneously recorded electrosensory pyramidal cells in the hindbrain of weakly electric fish. These cells constitute the output neurons of the first central nervous stage of electrosensory processing. Using random amplitude modulations (RAMs) of a mimic of the fish's own electric field within behaviorally relevant frequency bands, we found that pyramidal cells with overlapping receptive fields exhibit strong stimulus-induced correlations. To quantify the encoding of the RAM time course, we estimated the stimuli from simultaneously recorded spike trains and found significant improvements over single spike trains. The quality of stimulus reconstruction, however, was still inferior to the one measured for single primary sensory afferents. In an analysis of feature extraction, we found that spikes of pyramidal cell pairs coinciding within a time window of a few milliseconds performed significantly better at detecting upstrokes and downstrokes of the stimulus compared with isolated spikes and even spike bursts of single cells. Coincident spikes can thus be considered “distributed bursts.” Our results suggest that stimulus encoding by primary sensory afferents is transformed into feature extraction at the next processing stage. There, stimulus-induced coincident activity can improve the extraction of behaviorally relevant features from the stimulus.

THE NEURONAL BASIS of consciousness is the greatest challenge to the scientific worldview. Much relevant empirical work is carried out on the minimal neuronal mechanisms underlying any one specific conscious percept. Two broad approaches are popular among brain scientists: electrophysiological recordings from individual neurons in the cortex of behaving monkeys or behavior combined with functional brain imaging in humans. However, many aspects of consciousness are problematic or remain off-limits to the former approach, while the latter one lacks sufficient spatial and temporal resolution to monitor individual neurons that are key to perception, thought, memory, and action. It is here that neurosurgeons, probing the living human brain on a daily basis, can play a decisive role. This article explores the contributions of neurosurgeons to this quest and outlines some of the results that have already been achieved.

The directness and vivid quality of conscious experience belies the complexity of the underlying neural mechanisms, which remain incompletely understood. Recent work has focused on identifying the brain structures and patterns of neural activity within the primate visual system that are correlated with the content of visual consciousness. Functional neuroimaging in humans and electrophysiology in awake mokeys indicate that there are important differences between striate and extrastriate visual cortex in how well neural activity correlates with consciousness. Moreover, recent neuroimaging studies indicate that, in addition to these ventral areas of visual cortex, dorsal prefrontal and parietal areas might contribute to conscious visual experience.