Introduction suggests that each class of cell is responsible for carrying a

Brain Research 882 2000 241–250 www.elsevier.com locate bres Interactive report Functional plasticity in extrastriate visual cortex following neonatal 1 visual cortex damage and monocular enucleation a , a b c d Kurt R. Illig , Yuri P. Danilov , Aneeq Ahmad , Charlene B.Y. Kim , Peter D. Spear a Department of Anatomy and Centre for Neuroscience , University of Wisconsin Medical School, 1300 University Avenue, Madison, WI 53706, USA b Laboratory of Membrane Biochemistry and Biophysics , National Institute on Alcohol Abuse and Alcoholism, Rockville, MD 20852, USA c Department of Ophthalmology and Visual Sciences , University of Wisconsin, Madison, WI 53792, USA d Department of Psychology , University of Colorado, Boulder, CO 80309-0275, USA Accepted 10 September 2000 Abstract Neonatal lesions of primary visual cortex areas 17, 18 and 19; VC in cats lead to significant changes in the organization of visual pathways, including severe retrograde degeneration of retinal ganglion cells of the X b class. Cells in posteromedial lateral suprasylvian PMLS cortex display plasticity in that they develop normal receptive-field properties despite these changes, but they do not acquire the response properties of striate neurons that were damaged e.g., high spatial-frequency tuning, low contrast threshold. One possibility is that the loss of X-pathway information, which is thought to underlie striate cortical properties in normal animals, precludes the acquisition of these responses by cells in remaining brain areas following neonatal VC damage. Previously, we have shown that monocular enucleation at the time of VC lesion prevents the X- b-cell loss in the remaining eye. The purpose of the present study was to determine whether this sparing of retinal X-cells leads to the development of striate-like response properties in PMLS cortex. We recorded the responses of PMLS neurons to visual stimuli to assess spatial-frequency tuning, spatial resolution, and contrast threshold. Results indicated that some PMLS cells in animals with a neonatal VC lesion and monocular enucleation displayed a preference for higher spatial frequencies, had higher spatial resolution, and had lower contrast thresholds than PMLS cells in cats with VC lesion alone. Taken together, these results suggest that preserving X-pathway input during this critical period leads to the addition of some X-like properties to PMLS visual responses.  2000 Elsevier Science B.V. All rights reserved. Theme : Sensory systems Topic : Visual cortex: extrastriate Keywords : Posteromedial lateral suprasylvian; Plasticity; Visual cortex damage; X-pathway

1. Introduction suggests that each class of cell is responsible for carrying a

particular type of information into the visual system. In the mammalian eye, at least three types of retinal Further, the physiological properties of cells in different ganglion cells RGCs have been identified on the basis of cortical areas tend to reflect the input they receive. anatomical and physiological studies [2,5,6,9,17,19,20,32, Receptive-field characteristics of most area 17 cortical 33,38]. Termed X-, Y-, and W-cells, each of these primary cells have properties like X-cells in that they respond to RGC types projects to corresponding cells in the dorsal high spatial frequencies, have high spatial resolution, and lateral geniculate nucleus dLGN, which in turn project to have low contrast thresholds. Responses of cells in areas primary visual cortex. The functional segregation and 18 and 19 are more like those of Y- and W-cells in that parallel organization of these three major input pathways they respond preferentially to low spatial frequencies, have low spatial resolution, and have high contrast thresholds [3,8,12,22,23,26,36,37]. 1 Published on the World Wide Web on 25 September 2000. Removal of primary visual cortex areas 17, 18 and 19; Corresponding author. Tel.: 11-608-262-1607; fax: 11-608-262- VC in the neonatal cat leads to significant changes in 7306. E-mail address : krilligfacstaff.wisc.edu K.R. Illig. remaining visual structures, including retrograde degenera- 0006-8993 00 – see front matter  2000 Elsevier Science B.V. All rights reserved. P I I : S 0 0 0 6 - 8 9 9 3 0 0 0 2 9 0 2 - 4 242 K tion of the dLGN and transneuronal retrograde degenera- to examine the physiological response properties of PMLS tion of RGCs [4,25,27,40]. The loss of dLGN cells is cortical cells in animals that received a VC lesion and severe; in adult cats that received a VC lesion on the day of monocular enucleation on the day of birth. Specifically, we birth, the volume of the dLGN is only 14 of that in recorded PMLS cell responses to visual stimuli in VC- normal adult cats [15]. Cells that remain have an anomal- lesion animals that had one eye removed at the time of the ous projection to postero-medial lateral suprasylvian lesion to investigate whether X-like response properties PMLS extrastriate cortex [7,15,16,24,31]. would develop in PMLS cortex, thereby making PMLS The degeneration of cells in the retina also is severe cortex more like striate cortex. We hypothesized that following neonatal VC damage, but it appears to be sparing retinal X-cells after a neonatal VC lesion would restricted to a single class of RGCs. Following a VC lesion lead to a novel extrastriate X-pathway input along the on the day of birth, nearly 80 of physiologically iden- enhanced geniculo-PMLS pathway and that this novel tified retinal X-cells are lost, whereas there is little or no projection would lead to changes in response properties in loss of Y- or W-cells [27,39,40]. Correspondingly, a loss of PMLS cortical cells that would reflect this novel input, up to 80 of cells with medium-sized somata has been including higher spatial-frequency tuning, higher spatial observed following a VC lesion within 1 week of birth resolution, and higher contrast sensitivity compared to [14,25]. normal PMLS cells. Physiological studies of extrastriate cortical neurons provide evidence that some functional reorganization accompanies the changes observed in the retina and dLGN following a neonatal VC lesion [31]. Most cells in normal

2. Materials and methods