Reliable and Precise Neuronal Firing during Sensory Plasticity in Superficial Layers of Primary Somatosensory Cortex

Abstract

Neocortical neurons show astonishing variation in the presence and timing of action potentials across stimulus trials, a phenomenon whose function and significance has been the subject of great interest. Here we present data showing that this response variability can be significantly reduced by altered sensory experience. Removal of all but one whisker from the side of the mouse face results in the rapid (within 24 h) potentiation of mean firing rates within the cortical representation of the spared whisker in young postnatal animals (postnatal days 13-16). Analysis of single-unit responses from whisker-spared animals shows that this potentiation can be attributed to an enhancement of trial-to-trial reliability (i.e., reduced response failures), as well as an increase in the mean number of spikes evoked within a successful trial. Changes were confined to superficial layers 2/3 and were not observed in the input layer of the cortex, layer 4. In addition to these changes in firing rates, we also observed profound changes in the precise timing of sensory-evoked responses. Trial-totrial temporal precision was enhanced and the absolute latency of responses was reduced after single-whisker experience. Enhanced spike-timing precision and trial-to-trial reliability could also be triggered in adolescent animals with longer periods (7 d) of singlewhisker experience. These experiments provide a quantitative analysis of how sensory experience can enhance both reliability and temporal precision in neocortical neurons and provide a framework for testing specific hypotheses about the role of response variability in cortical function and the molecular mechanisms underlying this phenomenon.

Experience-Dependent Plasticity of the Barrel Cortex in Mice Observed with 2-DG Brain Mapping and c-Fos: Effects of MMP-9 KO

“…This result is consistent with electrophysiological data of Benedetti et al (2009), who showed that removing of all but one whisker on one side of the snout results in the potentiation of stimulus-evoked firing in layer 2/3 neurons within the cortical representation of the spared whisker in adolescent mice after 7 days of deprivation. We did not observe further increase in c-Fos expression after 28 days of deprivation, which suggests that enhancement of the spared whiskers input reaches its maximum level already after 7 days of deprivation.…”

“…Potentiation of layer IV neurons responses in spared barrels was not observed with extracellular recordings in urethane anesthesia (Benedetti et al 2009). As with the 2-DG method, a significant proportion of the label is ascribed to synaptic activity (Schwartz et al 1979;Nudo and Masterton 1986), the signal in layer IV may originate from thalamocortical axons (Lu¨bke et al 2003;Meyer et al 2010), and interbarrel connections or from axons of layer IV making synapses on basal dendrites of layers II/III neurons (Meyer et al 2010).…”

Natural Movies Evoke Spike Trains with Low Spike Time Variability in Cat Primary Visual Cortex

“…and certain patterns of neuronal activity in the sensory system. In contrast to this notion, previous studies in visual cortex have found high variability in spike counts to repeated stimulus presentations (Schiller et al, 1976;Tolhurst et al, 1983;Vogels et al, 1989;Buracas et al, 1998) (but see Gur et al, 1997;Kara et al, 2000;DeWeese et al, 2003;Amarasingham et al, 2006;Gur and Snodderly, 2006;Nawrot et al, 2008;Benedetti et al, 2009). In fact, the Fano factor (FF), the ratio of the variance of the spike counts across repetitions to the mean spike count, was often found to be higher than that of a random Poisson process, which has a FF of 1.…”

“…A number of studies have uncovered sub-Poissonian spike count variability in diverse cortical areas (DeWeese et al, 2003;Uzzell and Chichilnisky, 2004;Gur and Snodderly, 2006;Benedetti et al, 2009;Maimon and Assad, 2009). However, Poisson-type variability was shown by Beck et al (2008) to enable the brain to make optimal Bayesian decisions.…”

“…In fact, the Fano factor (FF), the ratio of the variance of the spike counts across repetitions to the mean spike count, was often found to be higher than that of a random Poisson process, which has a FF of 1. The variability in spike times has also been shown to be quite high (Tomko and Crapper, 1974;Shadlen and Newsome, 1998;McAdams and Maunsell, 1999;Tolhurst et al, 2009) (but see Richmond and Optican, 1990;McClurkin et al, 1991;Bair and Koch, 1996;Buracas et al, 1998;Nawrot et al, 2008;Benedetti et al, 2009;Maimon and Assad, 2009). As a result, neuronal responses have often been modeled using a nonuniform Poisson process, in which the probability of a spike or the firing rate would be constant for a short time window, and then change to a different rate as a function of the stimulus (Victor and Purpura, 1996;Berry and Meister, 1998;Oram et al, 1999).…”