Neonatal Cortical Ablation Disrupts Multisensory Development in Superior Colliculus

Abstract

ablation disrupts multisensory development in superior colliculus. J Neurophysiol 95: 1380 -1396, 2006. First published November 2, 2005 doi:10.1152/jn.00880.2005. The ability of cat superior colliculus (SC) neurons to synthesize information from different senses depends on influences from two areas of the cortex: the anterior ectosylvian sulcus (AES) and the rostral lateral suprasylvian sulcus (rLS). Reversibly deactivating the inputs to the SC from either of these areas in normal adults severely compromises this ability and the SC-mediated behaviors that depend on it. In this study, we found that removal of these areas in neonatal animals precluded the normal development of multisensory SC processes. At maturity there was a substantial decrease in the incidence of multisensory neurons, and those multisensory neurons that did develop were highly abnormal. Their cross-modal receptive field register was severely compromised, as was their ability to integrate cross-modal stimuli. Apparently, despite the impressive plasticity of the neonatal brain, it cannot compensate for the early loss of these cortices. Surprisingly, however, neonatal removal of either AES or rLS had comparatively minor consequences on these properties. At maturity multisensory SC neurons were quite common: they developed the characteristic spatial register among their unisensory receptive fields and exhibited normal adult-like multisensory integration. These observations suggest that during early ontogeny, when the multisensory properties of SC neurons are being crafted, AES and rLS may have the ability to compensate for the loss of one another's cortico-collicular influences so that normal multisensory processes can develop in the SC.

Brief Cortical Deactivation Early in Life Has Long-Lasting Effects on Multisensory Behavior

“…This deficit was manifested behaviorally as an absence of cross-modal facilitation in a simple localization task. The results are consistent with the hypothesis that association cortex must be functional for the brain to use cross-modal experience to craft the midbrain circuit underlying multisensory enhancement in orientation and localization tasks (Wallace and Stein, 1997;Jiang et al, 2002Jiang et al, , 2006Jiang et al, , 2007Yu et al, 2013). Although there is little direct information regarding the specific biophysical mechanisms involved in this maturational process, one prominent hypothesis is that a basic Hebbian mechanism is at work, either via projections from cortex to SC or via recurrent loops.…”

“…Furthermore, their expression in the adult animal depends on the integrity of influences that converge from different unisensory neurons of ipsilateral association cortex (i.e., the anterior ectosylvian sulcus [AES]; and the rostral lateral suprasylvian sulcus [rLS]) (Wallace et al, 1993;Jiang et al, 2001;Alvarado et al, 2007Alvarado et al, , 2009. Depriving the developing animal of relevant cross-modal experience or depriving the adult SC of these cortical influences has similar deleterious effects on the responses of individual SC neurons and the expression of SC-mediated behavior: stimuli from the different sensory modalities elicit appropriate responses, but their crossmodal combinations cannot be integrated to produce response enhancement (Jiang et al, 2002;Wallace et al, 2004;Yu et al, 2010;Xu et al, 2012).…”

The Development of Cortical Multisensory Integration

“…The sensory chronology of AES appears to follow a pattern closely paralleling that found in its major subcortical target structure, the SC (Stein et al, 1973). This midbrain structure plays a central role in the transformation of sensory signals into premotor commands (Sparks, 1986;Stein and Meredith, 1993) and depends on AES for its ability to integrate cross-modal inputs to amplify its sensory responses and the behaviors that depend on them (Stein et al, 1989;Wallace et al, 1993;Wilkinson et al, 1996;Wallace and Stein, 2000;Jiang et al, 2001Jiang et al, , 2002Jiang et al, , 2006. Finally, much like the SC , the appearance of the amplified multisensory integrative product in any given AES neuron appeared to be an all-or-none event.…”

“…Thus, the AES appears to coordinate the maturation of multisensory capabilities in its intrinsic neurons, presumably involved in higherorder functions, with those of its target neurons in the SC through which it controls orientation behaviors (Wallace and Stein, 2000;Jiang et al, 2006). Furthermore, it appears to exercise this coordination late in the period during which cross-modal experiences critical for multisensory integration are acquired (Wallace et al, 2004b;Wallace and Stein, 2006).…”

“…Although there is substantial development of AES after birth, the sulcus is already well formed and clearly evident before the second week of postnatal life (Jiang et al, 2006). Recording experiments began with animals 4 weeks after birth and at 4 week intervals thereafter, resulting in sampling at 4 (n ϭ 4), 8 (n ϭ 4), 12 (n ϭ 3), 16 (n ϭ 3), and 20 (n ϭ 2) weeks of age, as well as in adults (n ϭ 3).…”