Abstract
SummaryIn order to explore and interact with their surroundings, animals need to orient toward specific positions in space. Throughout the animal kingdom, head movements represent a primary form of orienting behavior. The superior colliculus (SC) is a fundamental structure for the generation of orienting responses, but how genetically distinct groups of collicular neurons contribute to these spatially tuned behaviors remains largely to be defined. Here, through the genetic dissection of the murine SC, we identify a functionally and genetically homogeneous subclass of glutamatergic neurons defined by the expression of the paired-like homeodomain transcription factor Pitx2. We show that the optogenetic stimulation of Pitx2ON neurons drives three-dimensional head displacements characterized by stepwise, saccade-like kinematics. Furthermore, during naturalistic foraging behavior, the activity of Pitx2ON neurons precedes and predicts the onset of spatially tuned head movements. Intriguingly, we reveal that Pitx2ON neurons are clustered in an orderly array of anatomical modules that tile the entire intermediate layer of the SC. Such a modular organization gives origin to a discrete and discontinuous representation of the motor space, with each Pitx2ON module subtending a defined portion of the animal’s egocentric space. The modularity of Pitx2ON neurons provides an anatomical substrate for the convergence of spatially coherent sensory and motor signals of cortical and subcortical origins, thereby promoting the recruitment of appropriate movement vectors. Overall, these data support the view of the superior colliculus as a selectively addressable and modularly organized spatial-motor register.
Highlights
In order to successfully interact with the environment, animals need to produce orienting movements toward specific positions in space
We identify a subpopulation of glutamatergic projecting neurons located in the stratum griseum intermediale (SGI) and defined by the expression of the paired-like homeodomain transcription factor Pitx2 [25], accounting for approximately half of the local glutamatergic population
We show that individual Pitx2ON units are tuned to specific head displacement vectors and that their optogenetic activation is sufficient to trigger stereotyped head orienting movements characterized by stepwise kinematics
Summary
In order to successfully interact with the environment, animals need to produce orienting movements toward specific positions in space Whether it is to hit a tennis ball or to shift our gaze toward an approaching threat, we are in constant need of planning and performing spatially accurate motor plans to match our goals. This process requires the convergence of target-related and internally generated signals onto a motor output network able to produce appropriate movement vectors Meaningful integration of this information is what creates the relational map that transforms object location, as probed by the senses, in motor coordinates, defining our ability to interact with the world around us and giving origin to our sense of space [1, 2]. A proportion of neurons in these layers display motor-related activity, being directly involved in the initiation of spatially accurate motor programs [10,11,12]
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