Contribution of Feedforward Thalamic Afferents and Corticogeniculate Feedback to the Spatial Summation Area of Macaque V1 and LGN ALESSANDRA ANGELUCCI * AND KESI SAINSBURY Department of Ophthalmology and Visual Science, Moran Eye Center, University of Utah, Salt Lake City, Utah 84132 ABSTRACT Neurons in the primary visual cortex (V1) respond best to oriented gratings of optimal size within their receptive field (RF) and are suppressed by larger gratings involving the nonclassical RF surround. A V1 neuron’s optimal stimulus size is larger at lower stimulus contrast. A central question in visual neuroscience is what circuits generate the size tuning of V1 cells. We recently demonstrated that V1 horizontal connections integrate signals within a region of the RF center corresponding to the V1 neuron’s optimal stimulus size at low contrast; extrastriate feedback connections to V1, instead, are longer range and can integrate signals from the most distant regions of the V1 cell’s RF surround. Here, we have determined the contribution of geniculocor- tical feedforward and corticogeniculate feedback connections to the size-tuning of macaque V1 and lateral geniculate (LGN) neurons, respectively. Specifically, we have quantitatively com- pared the visuotopic extent of geniculate feedforward afferents to V1 with the size of the RF center and surround of neurons in the V1 input layers and the visuotopic extent of V1 feedback connections to the LGN with the RF size of cells in V1 layer 6, where these connections originate. We find geniculate feedforward connections to provide visuotopic information to V1 that is spatially coextensive with the V1 neuron’s optimal stimulus size measured with high-contrast gratings. V1 feedback connections restrict their influence to an LGN region visuotopically coex- tensive with the size of the minimum response field (or classical RF) of V1 layer 6 cells and commensurate with the LGN region from which they receive feedforward connections. J. Comp. Neurol. 498:330 –351, 2006. © 2006 Wiley-Liss, Inc. Indexing terms: geniculocortical; lateral geniculate; primary visual cortex; primate; receptive field; surround Neurons in the primary visual cortex (V1) are tuned to the size of a visual stimulus; i.e., they respond best to oriented stimuli of optimal size (DeAngelis et al., 1994; Sceniak et al., 2001; Cavanaugh et al., 2002b; Levitt and Lund, 2002). This size-tuning is contrast dependent; i.e., the summation receptive field (RF) 1 is about twice as large at low contrast than when measured by using high- contrast gratings (Sengpiel et al., 1997; Kapadia et al., 1999; Sceniak et al., 1999). We refer to the diameter of the summation RF measured at high or low stimulus contrast as the cell’s high- or low-contrast summation RF (hsRF or lsRF) size, respectively (see Fig. 1). The summation RF is a high-threshold depolarizing region (Bringuier et al., 1999) surrounding the low-threshold spiking region of the RF center, i.e., the minimum response field (mRF; see Fig. 1) or classical RF (Barlow et al., 1967). Gratings of optimal orientation extending beyond the lsRF, into the surround (see Fig. 1), usually suppress the RF center’s response (Blakemore and Tobin, 1972; Nelson and Frost, 1978; All- man et al., 1985; Gilbert and Wiesel, 1990; DeAngelis et al., 1994). The circuitry generating the size-tuning of V1 cells remains to be identified. Recent studies have demonstrated that V1 horizontal connections are spatially coextensive with the size of V1 Grant sponsor: National Science Foundation; Grant number: IBN 0344569; Grant sponsor: National Eye Institute; Grant number: EY 015262; Grant sponsor: University of Utah Research Foundation; Grant sponsor: Research to Prevent Blindness (to the Department of Ophthal- mology, University of Utah). *Correspondence to: Alessandra Angelucci, Department of Ophthalmol- ogy and Visual Science, Moran Eye Center, University of Utah, 50 North Medical Drive, Salt Lake City, UT 84132. E-mail: alessandra.angelucci@hsc.utah.edu Received 17 February 2006; Revised 21 April 2006; Accepted 25 April 2006 DOI 10.1002/cne.21060 Published online in Wiley InterScience (www.interscience.wiley.com). THE JOURNAL OF COMPARATIVE NEUROLOGY 498:330 –351 (2006) © 2006 WILEY-LISS, INC.