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The Journal of Neuroscience, July 25, 2007, 27(30):8112-8121; doi:10.1523/JNEUROSCI.1420-07.2007

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Behavioral/Systems/Cognitive
A Cholinergic Gating Mechanism Controlled by Competitive Interactions in the Optic Tectum of the Pigeon

Gonzalo Marín,¹ Carlos Salas,¹ Elisa Sentis,¹ Ximena Rojas,² Juan Carlos Letelier,¹ and Jorge Mpodozis¹

¹Departamento de Biología, Facultad de Ciencias and ²Programa de Morfología, Facultad de Medicina, Universidad de Chile, Santiago, Chile

Correspondence should be addressed to Gonzalo Marín, Departamento de Biología, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Ñuñoa, Santiago, Chile. Email: gmarin{at}uchile.cl

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.

Key words: spatial attention; cholinergic; winner-take-all; optic tectum; superior colliculus; isthmi

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Received March 29, 2007; revised May 30, 2007; accepted June 18, 2007.

Correspondence should be addressed to Gonzalo Marín, Departamento de Biología, Facultad de Ciencias, Universidad de Chile, Las Palmeras 3425, Ñuñoa, Santiago, Chile. Email: gmarin{at}uchile.cl

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