Individual cortical neurons can selectively respond to specific environmental features, such as visual motion or faces. How this relates to the selectivity of the presynaptic network across cortical layers remains unclear. We used single-cell-initiated, monosynaptically restricted retrograde transsynaptic tracing with rabies viruses expressing GCaMP6s to image, in vivo, the visual motion-evoked activity of individual layer 2/3 pyramidal neurons and their presynaptic networks across layers in mouse primary visual cortex. Neurons within each layer exhibited similar motion direction preferences, forming layer-specific functional modules. In one-third of the networks, the layer modules were locked to the direction preference of the postsynaptic neuron, whereas for other networks the direction preference varied by layer. Thus, there exist feature-locked and feature-variant cortical networks.

We study the integration of multisensory and central input at the level of an identified fly motoneuron, the ventral cervical nerve motoneuron (VCNM) cell, which controls head movements of the animal. We show that this neuron receives input from a central neuron signaling flight activity, from two identified wide-field motion-sensitive neurons, from the wind-sensitive Johnston organ on the antennae, and from the campaniform sensillae of the halteres. We find that visual motion alone leads to only subthreshold responses. Only when it is combined with flight activity or wind stimuli does the VCNM respond to visual motion by modulating its spike activity in a directionally selective way. This nonlinear enhancement of visual responsiveness in the VCNM by central activity is reflected at the behavioral level, when compensatory head movements are measured in response to visual motion. While head movements of flies have only a small amplitude when flies are at rest, the response amplitude is increased by a factor of 30-40 during flight.behavioral state | electrophysiology | motion vision | proprioceptor T he perceptual response to a sensory stimulus depends on the behavioral state of the animal. This is especially evident when responses between awake and sleeping or anesthetized animals are compared (1-5). In addition, attention can strongly modulate the perceptual response (6-11). Furthermore, recent studies have shown that the response properties of sensory neurons depend on the locomotor state of the animal (12-16). However, it is not clear at what level of the nervous system the integration of sensory input and internal state occurs and according to which rules. We address this question in an identified ventral cervical nerve motoneuron (VCNM) that is part of the neck motor system of the blowfly Calliphora vicina.Blowflies are well known for their aerobatic maneuvers. This flight behavior has important consequences for vision, because fast turns can lead to motion blur and thus impair vision of spatial details. These adverse effects on vision can, in principle, be partly compensated for by eye movements. However, in all insects, the eyes are fixed to the head capsule and only small eye movements are possible (17). Therefore, effective compensatory eye movements can only be made by turning the head. Blowflies can turn their head relative to the thorax around all three body axes but with different amplitudes (yaw, ±20°; pitch, ±20°; and roll, ±90°). Accordingly, movements of the thorax during flight are compensated for by countermovements of the head relative to the thorax (18-21). These head movements are mediated by the neck motor system, which consists of 21 pairs of muscles, with each of them innervated by a single motoneuron (22,23). The three oblique horizontal muscles, OH3-5, are supplied by the ventral cervical nerve, comprising the axons of three identical motor neurons, . Unilateral contraction of these muscles leads to a sidewise deflection of the head (yaw response), whereas bilateral contraction pulls th...

Many motion-sensitive tangential cells of the lobula plate in blowflies are well described with respect to their visual response properties and the connectivity among them. They have large and complex receptive fields with different preferred directions in different parts of their receptive fields matching the optic flow that occurs during various flight maneuvers. However, much less is known about how tangential cells connect to postsynaptic neurons descending to the motor circuits in the thoracic ganglion and how optic flow is represented in these downstream neurons. Here we describe the physiology and the connectivity of a prominent descending neuron called DNOVS1 (for descending neurons of the ocellar and vertical system). We find that DNOVS1 is electrically coupled to a subset of vertical system cells. The specific wiring leads to a preference of DNOVS1 for rotational flow fields around a particular body axis. In addition, DNOVS1 receives input from interneurons connected to the ocelli.

For visual orientation and course stabilization, flies rely heavily on the optic flow perceived by the animal during flight. The processing of optic flow is performed in motion-sensitive tangential cells of the lobula plate, which are well described with respect to their visual response properties and the connectivity among them. However, little is known about the postsynaptic descending neurons, which convey motion information to the motor circuits in the thoracic ganglion. Here we investigate the physiology and connectivity of an identified premotor descending neuron, called DNOVS2 (for descending neuron of the ocellar and vertical system). We find that DNOVS2 is tuned in a supralinear way to rotation around the longitudinal body axis. Experiments involving stimulation of the ipsilateral and the contralateral eye indicate that ipsilateral computation of motion information is modified nonlinearly by motion information from the contralateral eye. Performing double recordings of DNOVS2 and lobula plate tangential cells, we find that DNOVS2 is connected ipsilaterally to a subset of vertical-sensitive cells. From the contralateral eye, DNOVS2 receives input most likely from V2, a heterolateral spiking neuron. This specific neural circuit is sufficient for the tuning of DNOVS2, making it probably an important element in optomotor roll movements of the head and body around the fly's longitudinal axis.