Early Bilateral Sensory Deprivation Blocks the Development of Coincident Discharge in Rat Barrel Cortex

Abstract

Several theories have proposed a functional role for synchronous neuronal firing in generating the neural code of a sensory perception. Synchronous neural activity develops during a critical postnatal period of cortical maturation, and severely reducing neural activity in a sensory pathway during this period could interfere with the development of coincident discharge among cortical neurons. Loss of such synchrony could provide a fundamental mechanism for the degradation of acuity shown in behavioral studies. We tested the hypothesis that synchronous discharge of barrel cortex neurons would fail to develop after sensory deprivation produced by bilateral whisker trimming from birth to postnatal day 60. By studying the correlated discharge of cortical neuron pairs, we found evidence for strong correlated firing in control animals, and this synchrony was almost absent among pairs of cortical barrel neurons in deprived animals. The degree of synchrony impairment was different in subregions of rat barrel cortex. The model that best fits the data is that cortical neurons receiving direct inputs from the primary sensory (lemniscal) pathway show the greatest decrement in synchrony following sensory deprivation, while neurons with diverse inputs from other areas of thalamus and cortex are relatively less affected in this dimension of cortical function.

Cross-Sensory Modulation of Primary Sensory Cortex Is Developmentally Regulated by Early Sensory Experience

“…Dynamic crosssensory plasticity is also well documented where plasticity refers to the ability of active sensory modalities to recruit or strongly modulate neurons in a deprived area of cortex (for review, see Bavelier and Neville, 2002). Sensory deprivation of a particular modality during development diminishes the response magnitude of the deprived neurons (Wiesel and Hubel, 1965;Simons and Land, 1987;Stern et al, 2001;Popescu and Ebner, 2010) and disrupts neuronal synchrony (Ghoshal et al, 2009) in primary cortical areas representing that modality. The net effect is that "deprived" cortical neurons become less responsive to natural stimuli.…”

Unilateral whisker trimming in newborn rats alters neuronal coincident discharge among mature barrel cortex neurons

“…In addition, data from the bilaterally whisker-trimmed rats (BD rats) used in Ghoshal et al (2009) were reanalyzed (data from layer II/III not shown in Ghoshal et al 2009) for comparison purposes. Whiskers were trimmed to the level of the fur using a head worn loupe for close observation for 60 days beginning at birth: the first 30 days (when the whisker growth rate was faster) the whiskers were trimmed every day, while after postnatal day 30 the whiskers were trimmed every other day.…”

“…Surgery and recordings were carried out under urethane anesthesia (1.5 g/kg ip, 30% solution), as described in Ghoshal et al (2009). In short, we used sets of three quartz glass insulated, platinum/iridium microelectrodes having 2-6 M⍀ resistance (Thomas Recording) that were advanced into cortex 305 m Fig.…”

“…Previously, almost all studies related to sensory deprivation have been focused on changes in receptive field architecture, response magnitude, and latency of the neurons. The effect of BD on spike timing and correlation between neurons showed that there are severe deficits in correlated discharge among adult barrel cortical neurons (Ghoshal et al 2009). Several theories of cortical coding include correlated discharge (neuronal synchrony) within neuronal ensembles as an important component of the neural code (Abbott and Dayan 1999;Eggermont 2001Eggermont , 2006Panzeri et al 2010).…”

“…Several theories of cortical coding include correlated discharge (neuronal synchrony) within neuronal ensembles as an important component of the neural code (Abbott and Dayan 1999;Eggermont 2001Eggermont , 2006Panzeri et al 2010). The synchrony is degraded more or less throughout all deprived subdivisions of primary sensory cortex following BD (Eggermont 2007;Ghoshal et al 2009). Thus the results from BD support the conclusion that, like the firing rate properties of neurons, the development of spontaneous spike synchrony is also activity dependent in rat cortex.…”