Unraveling Cross-Modal Development in Animals: Neural Substrate, Functional Coding and Behavioral Readout

in Multisensory Research
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The interaction of every living organism with its environment relies on sensory abilities. Hence, sensory systems need to develop rapidly and early in life to guarantee an individual’s survival. Sensors have to emerge that are equipped with receptors that detect a variety of stimuli. These sensors have to be wired in basic interconnected networks that possess the ability to process the uni- as well as multisensory information encoded in the sensory input. Plastic changes to refine and optimize these circuits need to be effected quickly during periods of sensory experience so that uni- and multisensory systems can rapidly achieve the functional maturity needed to support the perceptual and behavioral functions reliant upon them. However, the requirement that sensory abilities mature quickly during periods of enhanced neuroplasticity is at odds with the complexity of sensory networks. Neuronal assemblies within sensory networks must be precisely wired so that processing and coding mechanisms can render relevant stimuli more salient and bind features together appropriately. Focusing on animal research, the first part of this review describes mechanisms of sensory processing that show a high degree of similarity within and between sensory systems and highlight the network complexity in relationship to the temporal and spatial precision that is needed for optimal coding and processing of sensory information. Given the resemblance of most adult intra- and intersensory coding mechanisms, it is likely that their developmental principles are similar. The second part of the review focuses on developmental aspects, summarizing the mechanisms underlying the emergence and refinement of precisely coordinated neuronal and multisensory functioning. For this purpose, we review animal research that elucidates the neural substrate of multisensory development applicable to, the less accessible, human development. Animal studies in this field have not only complemented human studies, but brought new ideas and numerous cutting edge conclusions leading to the discovery of common principles and mechanisms.

Unraveling Cross-Modal Development in Animals: Neural Substrate, Functional Coding and Behavioral Readout

in Multisensory Research

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Figures

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    Rate, temporal and phase coding of sensory information in neuronal populations together with cross-modal modulation mechanisms. (A) Schematic drawing of a rat receiving visual information (green arrow) about a behaviorally-irrelevant object (trees) and a behaviorally-relevant object (approaching eagle) that is accompanied by tactile and auditory information (sound and vibrations, blue and red arrows). (B) Schematic drawing of neurons (population A/population B) in lower visual processing areas coding in their firing rate the presence of visual sub-features of the eagle and trees, and feeding this information to neurons in higher processing areas (population C) where integration takes place (rate coding). Cross-modal input (blue and red arrow) enhances the firing rate of single feeder neurons and thereby the salience of visual information from population A. (C) Schematic drawing of synchronized visual evoked activity in populations A and B (black lines) coding visual features of the object and thereby binding the action potential output to short time-windows where feeder neurons are depolarized, so that receiver neurons combine the simultaneous input (temporal coding). Due to cross-modal input to population A (blue and red arrow), the synchronization of electrical activity is increased (blue-red dotted line), rendering action potential timing more precise and information more salient. (D) Schematic drawing of synchronized neuronal activity of neurons in populations A and B (black lines) feeding information to population C, which shows stimulus-unrelated synchronization (black line) arriving in a neutral oscillatory phase (no depolarization/hyperpolarization in population C when input arrives, phase coding). Cross-modal input (blue and red arrow) resets the phase of spontaneous oscillations in population C (blue-red dotted line) so that input from population A arrives in a ‘good’, depolarized phase, whereas input from population B arrives during a ‘bad’ phase of inhibition.

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    Effects of cross-modal deprivation for the development of unisensory and multisensory networks. (A) Photomontage depicting a juvenile rat with highlighted somatosensory (whisker pad) and visual (retina) receptor surfaces as well as topographic maps in primary cortices. (B) Schematic drawing of the impact of visual deprivation (red cross) for the processing of tactile input (black arrow) in the primary sensory cortex of the deprived modality (primary visual cortex, V1). Note that V1 is responding to tactile stimulation. (C) Similar to (B) but in the primary sensory area of the non-deprived modality (primary somatosensory cortex, S1). Note that S1 is hypertrophic and shows altered tactile responses. (D) Similar to (B) but in a multisensory processing area (superior colliculus, SC). Note that the percentage of neurons responding to somatosensory or auditory stimulation increases.

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    Developmental course of sensory experience onsets with the potential critical periods for uni- and multisensory processing in the rat. (A) Timeline depicting developmental events in the rat controlling the course of uni- (cyan), cross- (magenta) and multimodal (yellow) induced experience-dependent as well as experience-independent (black) activity. (B) Schematic drawing of different developmental stages and potential critical periods along the timeline in (A). Note that during development the tactile system is the first one becoming fully functional (whiskers grow), followed by the auditory system (ears open) and finally by the visual system (eyes open). (C) Schematic drawing of uni- (cyan), cross- (magenta) and multimodal (yellow) input to somatosensory (blue), visual (green) and auditory (red) systems at the developmental stages from (B) that could be crucial for the development of unisensory processing. (D) Same as (C) but for multisensory processing.

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