Sensory input is required for callosal axon targeting in the somatosensory cortex

Abstract

BackgroundSensory input is generally thought to be necessary for refining and consolidating neuronal connections during brain development. We here report that cortical callosal axons in somatosensory cortex require sensory input for their target selection in contralateral cortex.ResultsEliminating sensory input to either hemisphere by unilateral transection of infraorbital nerve (ION) prevents target selection of callosal axons in contralateral cortex. Strikingly, blocking sensory input bilaterally, by simultaneously transecting both IONs, results in rescued callosal projection. In contrast, non-simultaneous bilateral ION transection has the same effect as unilateral transection. Similar results are obtained by lesion of whisker hair follicles. c-Fos-positive neurons in brain slices treated with KCl is decreased more in contralateral cortex with unilateral removal of sensory input, but decreased similarly in both cortices in mice with simultaneous bilateral removal of sensory input. Frequency of sEPSC of cortical neurons is also reduced in contralateral cortex with the unilateral removal of sensory input, but equally reduced on both sides with the bilateral removal of sensory input, suggesting that unbalanced bilateral sensory input might lead to mismatched neuronal activity between the two cortices and contribute to the formation of callosal projection.ConclusionOur data demonstrate a critical role of balanced bilateral somatosensory input in the formation of callosal connections, and thus reveal a new role of sensory input in wiring brain circuits.

The anatomy, organisation and development of contralateral callosal projections of the mouse somatosensory cortex

“…For example, regionspecific callosal projections are differentially affected by balanced activity across hemispheres (Huang et al, 2013;Suárez et al, 2014). Our findings of a dorsomedial to ventrolateral pattern of contralateral axon innervation are in accordance with previous findings, whereby contralateral innervation recapitulates the dorsoventral axonal arrangement within the callosal tract (Zhou et al, 2013).…”

Oxytocin is implicated in social memory deficits induced by early sensory deprivation in mice

“…This process is, however, extremely vulnerable to deleterious effects including sensory deprivation. In mice, transection of ION can lead to loss of barrel structures and callosal connection in the somatosensory cortex [5, 6, 22]. However, few studies have explored behavioral alterations beyond the whisker-related somatosensory system in these mice.…”

“…The alterations in the brain caused by the early sensory deprivation are not limited to loss of barrels. For example, the early sensory deprivation also affects synaptic plasticity [14, 15], dendritic spine refinement and formation of local circuitry [16–20], and inter-hemispheric in the somatosensory cortex [22]. We thus speculated the spatial memory and social memory deficits in ION-transected mice are the consequence of global structural and functional alterations in brain circuits after the early sensory deprivation.…”

“…Our previous studies have shown that early unilateral sensory deprivation impairs the formation of callosal projection between the bilateral somatosensory cortices [22]. Corpus callosum is involved in the communication of two hemispheres, which has been evidenced in patients with callosotomy (split-brain) by examination of latererized brain functions in dominant hemisphere [59, 60]; these higher brain functions could not examined in rodents.…”

“…In addition, callosal projections in the somatosensory cortex can be disrupted by unilateral transection of ION, and this disruption is permanent in adult brain, showing that early sensory input is also critical for the formation of inter-hemispheric connection in the cortex [22]. We thus hypothesized that the abnormal development of brain circuits caused by the early sensory deprivation may lead to alterations of adult behaviors.…”