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The Journal of Neuroscience, August 6, 2003, 23(18):7021-7033

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Selective Elimination of Corticogeniculate Feedback Abolishes the Electroencephalogram Dependence of Primary Visual Cortical Receptive Fields and Reduces Their Spatial Specificity

Dirk Eyding,¹ Jeffrey D. Macklis,^2,3,4 * Ute Neubacher,¹ Klaus Funke,^1 * and Florentin Wörgötter^5 *

¹Department of Neurophysiology, Ruhr University Bochum, D-44780 Bochum, Germany, ²Department of Neurology and Program in Neuroscience, Harvard Medical School, ³Division of Neuroscience, Children's Hospital, and ⁴Massachusetts General Hospital-Harvard Medical School Center for Nervous System Repair, Massachusetts General Hospital, Boston, Massachusetts 02115, and ⁵Department of Psychology, University of Stirling, Stirling FK9 4LA, United Kingdom

The role of corticogeniculate feedback in the organization, function, and state dependence of visual responses and receptive fields (RFs) is not well understood. We investigated the contribution of the corticogeniculate loop to state-dependent changes of characteristics of the primary visual cortex response by using a novel approach of eliminating corticogeniculate projection neurons with targeted neuronal apoptosis. Experiments were performed in anesthetized cats (N₂O plus halothane) with parallel recordings of single units from experimental (right) and control (left) hemispheres 2 weeks after induction of apoptosis. Within the experimental hemispheres, neurons of area 17 and of the dorsal lateral geniculate nucleus (dLGN) showed an unusually enhanced and prolonged tonic visual response during episodes of synchronized (syn) EEG activity, whereas response levels during less synchronized states were almost normal. In addition, dLGN cells showed a reduced tendency for burst firing and a less regular spike interval distribution compared with those of controls. These changes are likely attributable to a tonic depolarization of dLGN relay neurons or, more likely, to a decreased responsiveness of thalamic inhibitory processes to cortical feedback. Cortical neurons also displayed an activity-dependent increase in RF size, in contrast to an almost activity-invariant RF size of controls, a phenomenon likely related to the elimination of collateral, intracortical projections of layer 6 neurons. Together, these results demonstrate that selective chronic elimination of corticogeniculate feedback results in the loss of EEG-correlated differences of visual processing in the remaining thalamocortical network, accompanied by a significant increase in excitability during syn EEG, at the expense of noticeably reduced spatial receptive-field specificity in the remaining cortical neurons.

Key words: visual cortex; corticogeniculate loop; photoactivation of chlorin e₆; neuronal apoptosis; state dependence; receptive-field characteristics

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Received Nov. 1, 2002; revised May. 28, 2003; accepted May. 29, 2003.

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