Plasticity in adult cat visual cortex (area 17) following circumscribed monocular lesions of all retinal layers

Abstract

It has been shown in a number of previous studies that in adult cats discrete retinal lesions induce a reorganization of visuotopic maps in that part of striate cortex (area 17; V1) in which the lesioned part of the retina was represented (Kaas et al. 1990;Chino et al. 1992Chino et al. , 1995Gilbert & Wiesel, 1992;Darian-Smith & Gilbert, 1995;Schmid et al. 1995Schmid et al. , 1996Calford et al. 1999). Projected onto area 17, these lesions represented an area (lesion projection zone; LPZ) typically 3 to 5 mm in diameter, within which the visual receptive fields of many neurones were displaced to normal retina immediately adjacent to the lesioned retina. So far the studies of this issue have covered three experimental protocols: (1) matched homonymous retinal lesions have been made in the two eyes (Gilbert & Wiesel, 1992;Chino et al. 1995;Darian-Smith & Gilbert, 1995); (2) a retinal lesion has been placed in one eye while the other has been enucleated (Chino et al. 1992;Schmid et al. 1996); and (3) a retinal lesion has been made monocularly while the retina in the other eye remained intact (Chino, 1992;Schmid et al. 1996). The topographical extent of the retinal lesioninduced plasticity in the dorsal lateral geniculate nucleus (LGNd) is very small and therefore presumably incapable of providing a substrate for the extensive reorganization of the visuotopic map in the cortex (Eysel et al. 1981; DarianSmith & Gilbert, 1995). It is therefore generally agreed that the apparent topographic reorganization observed in studies with the 1st and 2nd experimental protocols, is based on plasticity at the cortical level and that the most likely source Journal of Physiology (2000) 1. In eight adult cats intense, sharply circumscribed, monocular laser lesions were used to remove all cellular layers of the retina. The extents of the retinal lesions were subsequently confirmed with counts of á_ganglion cells in retinal whole mounts; in some cases these revealed radial segmental degeneration of ganglion cells distal to the lesion. 2. Two to 24 weeks later, area 17 (striate cortex; V1) was studied electrophysiologically in a standard anaesthetized, paralysed (artificially respired) preparation. Recording single-or multineurone activity revealed extensive topographical reorganization within the lesion projection zone (LPZ). 3. Thus, with stimulation of the lesioned eye, about 75% of single neurones in the LPZ had 'ectopic' visual discharge fields which were displaced to normal retina in the immediate vicinity of the lesion. 4. The sizes of the ectopic discharge fields were not significantly different from the sizes of the normal discharge fields. Furthermore, binocular cells recorded from the LPZ, when stimulated via their ectopic receptive fields, exhibited orientation tuning and preferred stimulus velocities which were indistinguishable from those found when the cells were stimulated via the normal eye. 5. However, the responses to stimuli presented via ectopic discharge fields were generally weaker (lower peak discharge rates) tha...

Human Adult Cortical Reorganization and Consequent Visual Distortion

“…This finding corroborates the numerous animal studies suggesting that V1 retains a remarkable degree of plasticity even in adulthood (Kaas et al, 1990;Heinen and Skavenski, 1991;Gilbert and Wiesel, 1992;Chino et al, 1992;Darian-Smith and Gilbert, 1995;Schmid et al, 1996;Calford et al, 2000), and contradicts previous reports of no cortical reorganization in the adult animal visual system (Horton and Hocking, 1998;Smirnakis et al, 2005a). Additionally, our results support the finding of large-scale reorganization after deafferentation of human adult visual cortex in patients with macular degeneration (Baker et al, 2005).…”

“…Initial neural evidence came from adult animal studies in which a region of the primary visual cortex (V1) was deafferented by means of retinal lesions (Kaas et al, 1990;Heinen and Skavenski, 1991;Gilbert and Wiesel, 1992;Chino et al, 1992;Darian-Smith and Gilbert, 1995;Schmid et al, 1996;Calford et al, 2000). Like deafferented neurons in the S1, deafferented V1 neurons began responding to stimuli that normally activated the adjacent V1 cortex.…”

Functional and cortical adaptations to central vision loss

“…In summary, both cat and monkey studies provide evidence for retinotopic reorganization as a result of retinal deafferentation (Kaas et al, 1990;Heinen & Skavenski, 1991;Gilbert & Wiesel, 1992;Chino et al, 1992Chino et al, , 1995Darian-Smith & Gilbert, 1994, 1995Calford et al, 2000). Extensive reviews on cortical plasticity of sensory and motor organization can be found in Chino (1995), Gilbert (1998), and Kaas and Collins (2003).…”

“…Cat and monkey studies have shown that reorganization in adult mammalian visual cortex occurs following visual field loss (Kaas et al, 1990;Heinen & Skavenski, 1991;Gilbert & Wiesel, 1992;Chino et al, 1992Chino et al, , 1995Darian-Smith & Gilbert, 1994, 1995Calford et al, 2000). Prior to these studies, prevailing wisdom held that connections along the retinocortical visual pathways are very rigid following a developmental critical period (weeks old) (see Boothe et al, 1985 for a review).…”

The second face of blindness: Processing speed deficits in the intact visual field after pre- and post-chiasmatic lesions

“…Firstly, partial optic nerve damage or cortical tissue loss may lead to a reduced physiological signaling power and to a loss of firing synchrony of neuronal assemblies, thus increasing processing time. Secondly, there is an extensive remapping and reorganization of the visual field representation after pre-and post-chiasmatic damage as shown in animal model studies [34][35][36][37], as well as behavioral [38] and fMRI studies in patients [31][32][33]39]. Such receptive field reorganization is believed to be mediated by mechanisms involving plasticity of intrinsic cortical horizontal connections [40].…”