Abstract
Hemianopic patients exhibit visual detection improvement in the blind field when audiovisual stimuli are given in spatiotemporally coincidence. Beyond this “online” multisensory improvement, there is evidence of long-lasting, “offline” effects induced by audiovisual training: patients show improved visual detection and orientation after they were trained to detect and saccade toward visual targets given in spatiotemporal proximity with auditory stimuli. These effects are ascribed to the Superior Colliculus (SC), which is spared in these patients and plays a pivotal role in audiovisual integration and oculomotor behavior. Recently, we developed a neural network model of audiovisual cortico-collicular loops, including interconnected areas representing the retina, striate and extrastriate visual cortices, auditory cortex, and SC. The network simulated unilateral V1 lesion with possible spared tissue and reproduced “online” effects. Here, we extend the previous network to shed light on circuits, plastic mechanisms, and synaptic reorganization that can mediate the training effects and functionally implement visual rehabilitation. The network is enriched by the oculomotor SC-brainstem route, and Hebbian mechanisms of synaptic plasticity, and is used to test different training paradigms (audiovisual/visual stimulation in eye-movements/fixed-eyes condition) on simulated patients. Results predict different training effects and associate them to synaptic changes in specific circuits. Thanks to the SC multisensory enhancement, the audiovisual training is able to effectively strengthen the retina-SC route, which in turn can foster reinforcement of the SC-brainstem route (this occurs only in eye-movements condition) and reinforcement of the SC-extrastriate route (this occurs in presence of survived V1 tissue, regardless of eye condition). The retina-SC-brainstem circuit may mediate compensatory effects: the model assumes that reinforcement of this circuit can translate visual stimuli into short-latency saccades, possibly moving the stimuli into visual detection regions. The retina-SC-extrastriate circuit is related to restitutive effects: visual stimuli can directly elicit visual detection with no need for eye movements. Model predictions and assumptions are critically discussed in view of existing behavioral and neurophysiological data, forecasting that other oculomotor compensatory mechanisms, beyond short-latency saccades, are likely involved, and stimulating future experimental and theoretical investigations.
Highlights
The primary human visual pathway conveys the majority of retinal fibers to the lateral geniculate nucleus of the thalamus and via the optic radiations, to the primary visual cortex (V1)
The development of a basal oculomotor module including the FP input is relevant. In this way we provide an intact reference model that justifies the parameters of the collicular sensory-motor link used in pre-training condition and in synaptic learning in the simulated patients. (iii) Each trial starts with the simulated patient fixating centrally and can be performed in two different eye conditions: FixedEyes Condition, in which central fixation is hold, inhibiting any oculomotor response; Eye-Movements Condition, in which a saccade can be produced, shifting the gaze from the central fixation point toward the stimulus. (iv) The visual stimulus represents the target, while the auditory stimulus is an accessory stimulus
Hemianopic patients have been shown to benefit from audiovisual stimulation in an online temporary way (Frassinetti et al, 2005) and in an offline long-lasting way (Bolognini et al, 2005; Passamonti et al, 2009; Dundon et al, 2015b; Tinelli et al, 2015; Grasso et al, 2016)
Summary
The primary human visual pathway conveys the majority of retinal fibers to the lateral geniculate nucleus of the thalamus and via the optic radiations, to the primary visual cortex (V1) (the retino-geniculo-striate pathway). Results revealed a significant post-training improvement in detection of unimodal visual targets in the blind field when the patients were allowed to use eye movements, while a weak amelioration was found when they had to maintain central fixation (Bolognini et al, 2005; Tinelli et al, 2015). Such results suggest that the audiovisual training could promote an increased oculomotor response to visual stimuli in the affected hemifield. Different training paradigms (audiovisual multisensory/visual unisensory stimulation in eye-movements/fixed-eyes condition) are tested, to examine their efficacy in promoting different forms of rehabilitation (compensatory/restitutive), and to assess the predicted results in light of in vivo data
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