We describe the operation of a midbrain neural circuit in pigeons that may participate in selecting and attending to one visual stimulus from the myriad displayed in their visual environment. This mechanism is based on a topographically organized cholinergic signal reentering the optic tectum (TeO). We have shown previously that, whenever a visual stimulus activates neurons in a given tectal location, this location receives a strong bursting feedback from cholinergic neurons of the nucleus isthmi pars parvocellularis (Ipc), situated underneath the tectum. Here we show that, if a second visual stimulus is presented, even far from the first, the feedback signal to the first tectal location is diminished or suppressed, and feedback to the second tectal location is initiated. We found that this long-range suppressive interaction is mostly mediated by the nucleus isthmi pars magnocellularis, which sends a wide-field GABAergic projection to Ipc and TeO. In addition, two sets of findings indicate that the feedback from the Ipc modulates the ascending output from the TeO. First, visually evoked extracellular responses recorded in the dorsal anterior subdivision of the thalamic nucleus rotundus (RtDa), receiving the ascending tectal output, are closely synchronized to this feedback signal. Second, local inactivation of the Ipc prevents visual responses in RtDa to visual targets moving in the corresponding region of visual space. These results suggest that the ascending transmission of visual activity through the tectofugal pathway is gated by this cholinergic re-entrant signal, whose location within the tectal visual map is dynamically defined by competitive interactions.

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The retinotectofugal system is the main visual pathway projecting upon the telencephalon in birds and many other nonmammalian vertebrates. The ascending tectal projection arises exclusively from cells located in layer 13 of the optic tectum and is directed bilaterally toward the thalamic nucleus rotundus. Although previous studies provided evidence that different types of tectal layer 13 cells project to different subdivisions in Rt, apparently without maintaining a retinotopic organization, the detailed spatial organization of this projection remains obscure. We reexamined the pigeon tectorotundal projection using conventional tracing techniques plus a new method devised to perform small deep-brain microinjections of crystalline tracers. We found that discrete injections involving restricted zones within one subdivision retrogradely label a small fraction of layer 13 cells that are distributed throughout the layer, covering most of the tectal representation of the contralateral visual field. Double-tracer injections in one subdivision label distinct but intermingled sets of layer 13 neurons. These results, together with the tracing of tectal axonal terminal fields in the rotundus, lead us to propose a novel "interdigitating" topographic arrangement for the tectorotundal projection, in which intermingled sets of layer 13 cells, presumably of the same particular class and distributed in an organized fashion throughout the surface of the tectum, terminate in separate regions within one subdivision. This spatial organization has significant consequences for the understanding of the physiological and functional properties of the tectofugal pathway in birds.

Fast oscillatory bursts (OBs; 500 -600 Hz) are the most prominent response to visual stimulation in the optic tectum of birds. To investigate the neural mechanisms generating tectal OBs, we compared local recordings of OBs with simultaneous intracellular and extracellular single-unit recordings in the tectum of anesthetized pigeons. We found a specific population of units that responded with burst discharges that mirrored the burst pattern of OBs. Intracellular filling with biocytin of some of these bursting units demonstrated that they corresponded to the paintbrush axon terminals from the nucleus isthmi pars parvocellularis (Ipc). Direct recordings in the Ipc confirmed the high correlation between Ipc cell firing and tectal OBs. After injecting micro-drops of lidocaine in the Ipc, the OBs of the corresponding tectal locus disappeared completely. These results identify the paintbrush terminals as the neural elements generating tectal OBs. These terminals are presumably cholinergic and ramify across tectal layers in a columnar manner. Because the optic tectum and the Ipc are reciprocally connected such that each Ipc neuron sends a paintbrush axon to the part of the optic tectum from which its visual inputs come, tectal OBs represent re-entrant signals from the Ipc, and the spatial-temporal pattern of OBs across the tectum is the mirror representation of the spatial-temporal pattern of bursting neurons in the Ipc. We propose that an active location in the Ipc may act, via bursting paintbrushes in the tectum, as a focal "beam of attention" across tectal layers, enhancing the saliency of stimuli in the corresponding location in visual space.