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The Journal of Neuroscience, October 27, 2004, 24(43):9475-9485; doi:10.1523/JNEUROSCI.3289-04.2004

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Behavioral/Systems/Cognitive
Asymmetrical Modes of Visual Bottom-Up and Top-Down Integration in the Thalamic Nucleus Rotundus of Pigeons

Kristian Folta,1 Bettina Diekamp,2 and Onur Güntürkün1

1Institute for Cognitive Neuroscience, Department of Biopsychology, Faculty of Psychology, Ruhr-University Bochum, D-44780 Bochum, Germany, and 2Department of Psychological and Brain Sciences, Johns Hopkins University, Baltimore, Maryland 21218

The aim of this study was to separate bottom-up and top-down influences within cerebral asymmetries. This was studied in the lateralized visual system of pigeons by recording from single units of the left and right diencephalic nucleus rotundus of the tectofugal pathway while visually stimulating the ipsilateral and/or contralateral eye. Analyses of response latencies revealed rotundal neurons with short and/or late response components. Cells with short latencies very likely represent bottom-up neurons participating in the ascending retinotectorotundal system. Because lidocaine injections into the visual Wulst produced a significant reduction of late response components only, neurons with long latencies were probably activated via a top-down telencephalotectorotundal system. The distribution and response characteristics of bottom-up and top-down neurons provided insight into several asymmetries of ascending and descending pathways. Asymmetries of the ascending retinotectorotundal system (bottom-up) were characterized by longer periods of tonic activation in the left and shorter response latencies in the right rotundus. Left-right differences in these responses probably facilitate faster access to visual input to the right hemisphere and a prolonged processing of this input in the left. The descending telencephalotectorotundal system (top-down) revealed a completely different lateralized organization. This system was characterized by long latency responses that exclusively derived from the left hemisphere, regardless of whether recordings took place in the left or the right rotundus. We assume that asymmetrical modes of visual processing within both hemispheres of the ascending tectofugal system are ultimately directed to left hemispheric forebrain mechanisms that subsequently generate executive control over sensory and motor structures.

Key words: lateralization; birds; rotundus; visual system; tectofugal system; thalamofugal system


Received June 23, 2004; revised September 10, 2004; accepted September 10, 2004.




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