Neonatal Restriction of Tactile Inputs Leads to Long-Lasting Impairments of Cross-Modal Processing

Abstract

Optimal behavior relies on the combination of inputs from multiple senses through complex interactions within neocortical networks. The ontogeny of this multisensory interplay is still unknown. Here, we identify critical factors that control the development of visual-tactile processing by combining in vivo electrophysiology with anatomical/functional assessment of cortico-cortical communication and behavioral investigation of pigmented rats. We demonstrate that the transient reduction of unimodal (tactile) inputs during a short period of neonatal development prior to the first cross-modal experience affects feed-forward subcortico-cortical interactions by attenuating the cross-modal enhancement of evoked responses in the adult primary somatosensory cortex. Moreover, the neonatal manipulation alters cortico-cortical interactions by decreasing the cross-modal synchrony and directionality in line with the sparsification of direct projections between primary somatosensory and visual cortices. At the behavioral level, these functional and structural deficits resulted in lower cross-modal matching abilities. Thus, neonatal unimodal experience during defined developmental stages is necessary for setting up the neuronal networks of multisensory processing.

Rate and Temporal Coding Convey Multisensory Information in Primary Sensory Cortices

“…Neuronal firing precisely occurring during neuronal rhythms facilitates the transfer of information (Salinas and Sejnowski, 2001). While very few behavioral investigations addressed the S1–V1 interactions (Sieben et al, 2015), experimental evidence from auditory system supports this hypothesis (Alais and Cass, 2010; Gleiss and Kayser, 2012). Precise targeting and manipulation of neurons involved in interareal corticocortical communication is required in the future to understand the behavioral readout of their activity codes in multisensory perception.…”

“…Unimodal (either light flash or whisker deflection) or bimodal (simultaneous light flash and whisker deflection) stimuli were applied using a custom-made stimulation device as previously described (Sieben et al, 2013; Sieben et al, 2015). Briefly, whiskers were stimulated by deflection through compressed air-controlled roundline cylinders (RT/57110/M/10, Norgren) gated via solenoid valves (VCA, SMCPneumatik).…”

“…Retrograde tracer injections were performed as previously described (Sieben et al, 2015). In brief, ketamine/xylazine anesthetized rats were immobilized into a preformed mold fixed into the stereotaxic apparatus and received unilateral injections of the retrograde tracer Fluorogold (FG; Fluorochrome) in S1 barrel field (2.4-2.6 mm posterior and 5.5-5.8 mm lateral to bregma) or V1 (6.9-7.1 mm posterior and 3.4-3.7 mm lateral to bregma).…”

“…Modulation of network oscillations in their power and phase has been found to represent a powerful mechanism of cross-modal integration (Lakatos et al, 2007; Sieben et al, 2013). It seems to use as anatomic substrate not only thalamo-cortical projections (Zikopoulos and Barbas 2007, Lakatos et al, 2009) but also direct axonal projections between primary sensory cortices that have been documented across multiple species and areas (Falchier et al, 2002; Budinger et al, 2006; Hall and Lomber, 2008; Sieben et al, 2013; Stehberg et al, 2014; Zingg et al, 2014; Sieben et al, 2015). …”

Visual–tactile processing in primary somatosensory cortex emerges before cross‐modal experience

“…A custom‐built stimulation device placed in front of the animal was used to achieve unimodal (light‐flash, whisker deflection) or bimodal stimulation as described previously (Sieben et al, ). During bimodal stimulation, whisker deflection and light‐flashes (50 ms, 300 lx) were presented simultaneously in the same (congruent) or in opposite (incongruent) hemifields with respect to the tactile stimulus.…”