Abstract
Animals integrate the different senses to facilitate event-detection for navigation in their environment. In vertebrates, the optic tectum (superior colliculus) commands gaze shifts by synaptic integration of different sensory modalities. Recent works suggest that tectum can elaborate gaze reorientation commands on its own, rather than merely acting as a relay from upstream/forebrain circuits to downstream premotor centers. We show that tectal circuits can perform multisensory computations independently and, hence, configure final motor commands. Single tectal neurons receive converging visual and electrosensory inputs, as investigated in the lamprey - a phylogenetically conserved vertebrate. When these two sensory inputs overlap in space and time, response enhancement of output neurons occurs locally in the tectum, whereas surrounding areas and temporally misaligned inputs are inhibited. Retinal and electrosensory afferents elicit local monosynaptic excitation, quickly followed by inhibition via recruitment of GABAergic interneurons. Multisensory inputs can thus regulate event-detection within tectum through local inhibition without forebrain control.
Highlights
Sensorimotor circuits have been studied in a wide range of biological organisms in pursuit of identifying the operational principles that govern the integration of sensory information from different modalities for the generation of goal-directed behavior
The findings presented by Kardamakis, Perez-Fernandez and Grillner suggest that the optic tectum can direct attention to a particular event without requiring input from other brain areas
We show that visual and electroreceptive inputs are integrated in the same deep layer neurons of the optic tectum, which provide the output to different brainstem centers
Summary
Sensorimotor circuits have been studied in a wide range of biological organisms in pursuit of identifying the operational principles that govern the integration of sensory information from different modalities for the generation of goal-directed behavior. The optic tectum (superior colliculus in mammals), has received particular attention for its distinct role in orienting behavior, i.e. the control of orienting and avoidance gaze movements (Dean et al, 1989; Moschovakis et al, 1996; Basso and Wurtz, 1997; Sparks, 2002), through the integration of different sensory modalities (which are species-dependent) like vision, auditory and electroreception (Bodznick and Northcutt, 1981; Meredith and Stein, 1986; Wallace et al, 1996, Gingras et al, 2009). Studies of the superior colliculus have established a set of empirical principles that place constraints on the spatial and temporal dimensions underlying multisensory integration (Stein and Stanford, 2008). The goal of this study is to determine the cellular and synaptic mechanisms embedded within the optic tectum that control multisensory integration
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