The influence of different postnatal experiences on the integrative capabilities in the SC: a computational study

The midbrain superior colliculus (SC) integrates information from different senses (visual, auditory, somatosensory) to program orientation responses to external events. It derives the relevant sensory information from converging inputs from several cortical and subcortical structures. However, the SC does not integrate signals across the senses at birth, and acquires this capacity during development through interactions with cross-modal events. Protracted congenital pathological conditions can lead to a lack of integrative capabilities or the emergence of anomalous integration of cross-modal signals in the adult, suggesting that the mechanism that integrates these signals adapts to experience. The specific neural mechanisms underlying the maturation of the multisensory integration in the SC are not completely understood, but are believed to rely on inputs from specific areas of the cortex. Mathematical models are valuable in helping to clarify these ideas within a quantitative framework. We extended a neural network model of the adult SC (Cuppini et al., 2010) to describe the development of this phenomenon from the naïve to adult state. The naïve state of the model was based on known or suspected anatomy and physiology: 1) Cortical afferents are present but weak, 2) Responses are largely driven from afferents not derived from the cortex, and 3) The visual inputs have a marginal spatial tuning. Sensory experience was modelled by repeatedly simulating exposure to modality-specific and cross-modal stimuli by activating units in the cortical and non-cortical input layers. Synapses in the network were modified by a simple Hebbian learning rule. As a consequence of this exposure, 1) Receptive fields reduced in size, 2) Neurons became multisensory, and 3) Neurons gained the integrative properties characteristic of multisensory neurons in the SC: enhancement, depression, and inverse effectiveness. Importantly, the unique architecture of the model guided the development so that integration became dependent on the relationship between the cortical input and the SC. Manipulations of the statistics of the experience during the exposure phase changed the integrative profiles of the neurons, and the results matched well with the results of physiological studies. Supported by NIH Grants NS036916 and EY016716.