A neurochemical signature of visual recovery after extrastriate cortical damage in the adult cat

Abstract

In adult cats, damage to the extrastriate visual cortex on the banks of the lateral suprasylvian (LS) sulcus causes severe deficits in motion perception that can recover as a result of intensive direction discrimination training. The fact that recovery is restricted to trained visual field locations suggests that the neural circuitry of early visual cortical areas, with their tighter retinotopy, may play an important role in attaining perceptual improvements after damage to higher level visual cortex. The present study tests this hypothesis by comparing the manner in which excitatory and inhibitory components of the supragranular circuitry in an early visual cortical area (area 18) are affected by LS lesions and postlesion training. First, the proportion of LS-projecting pyramidal cells as well as calbindin-and parvalbumin-positive interneurons expressing each of the four AMPA receptor subunits was estimated in layers II and III of area 18 in intact animals. The degree to which LS lesions and visual retraining altered these expression patterns was then assessed. Both LS-projecting pyramidal cells and inhibitory interneurons exhibited long-term, differential reductions in the expression of glutamate receptor (GluR)1, -2, -2/3, and -4 following LS lesions. Intensive visual training post lesion restored normal AMPAR subunit expression in all three cell-types examined. Furthermore, for LS-projecting and calbindin-positive neurons, this restoration occurred only in portions of the ipsi-lesional area 18 representing trained visual field locations. This supports our hypothesis that stimulation of early visual cortical areas-in this case, area 18-by training is an important factor in restoring visual perception after permanent damage to LS cortex. Indexing termsGluR1; GluR2; GluR3; GluR4; NR1; calbindin; parvalbumin; pyramidal cellThe adult brain exhibits remarkable plasticity throughout life (see reviews by Gilbert et al., 1996;Kaas, 1995). Well-documented cases of training-induced recovery following damage to adult motor cortex (see reviews by Hallett, 2001;Cauraugh and Summers, 2005), adult somatosensory cortex (Xerri, 1998;Xerri et al., 2004), and adult visual cortex (Newsome and Pare, 1988; Pasternak, 1996, 1999;Huxlin and Pasternak, 2004) suggest that some of this plasticity can be tapped for the purpose of recovering function after permanent brain damage. In the visual system, most studies reporting training-induced recovery of function were conducted following damage to extrastriate visual cortex-lesions of the lateral suprasylvian (LS) visual cortex in cats, e.g. (Rudolph and Pasternak, 1996 Pasternak, 2004) or lesions in areas MT/MST of monkeys (Newsome and Pare, 1988;Rudolph and Pasternak, 1999).The feline LS cortex is a complex of extrastriate visual areas (Palmer et al., 1978;Sherk, 1986b;Grant and Shipp, 1991;Sherk and Mulligan, 1993) that exhibit functional similarity with areas MT/MST of primates (Payne, 1993), playing an important role in the processing of complex visual motion information (Rau...

Different Properties of Visual Relearning after Damage to Early Versus Higher-Level Visual Cortical Areas

“…6E, F). The DR relearning in cats with LS lesions replicated previous work from our laboratory (Huxlin and Pasternak, 2004; Huxlin et al, 2008). Similarly, when training was administered using stimuli in which coherence was varied, coherence thresholds progressively improved back to normal levels (Fig.…”

“…Cats were first taught to perform a left–right direction discrimination task using random dot stimuli and controlled fixation (see below) presented centrally until (1) they had learned the task and (2) their direction range (DR) thresholds reached stable levels (< 10% coefficient of variation over a 5 d period). In cats, normal DR thresholds range between 11 and 35% (Huxlin and Pasternak, 2004; Huxlin et al, 2008). Stimuli were then placed at 5–10 nonoverlapping, peripheral visual field locations of up to 20° eccentricity (in both hemifields of vision for the eight prelesion cats and in the intact, ipsilesional hemifield in the three postlesion cats) to ensure that cats were able to perform the task with normal thresholds at a range of visual field locations.…”

“…Random-dot stimuli, in which either the range of dot directions or the percentage coherence was varied, were used to measure the cats’ DR and coherence thresholds, as described previously (Huxlin and Pasternak, 2004; Huxlin et al, 2008). Each stimulus consisted of small dots (0.03° in diameter) presented within a circular aperture 4° in diameter.…”

“…The separation of the injections and the amount and concentration of ibotenic acid injected were previously shown to produce large, contiguous lesions of the desired visual cortical areas (Huxlin and Pasternak, 2001, 2004; Huxlin et al, 2008). The animals’ EKG, CO 2 , and temperature were constantly monitored during the surgery and kept at physiological levels.…”

Should Visual Restoration Therapy be Used in Patients With Visual Field Loss?

“…Evidence for neuroplasticity has been obtained from animal studies showing recovery of visual field loss after visual deprivation in young (4) and adult animals (5)(6)(7), and these experiments, in part, generated initial and continuing interest in human visual field restoration. Using a suprathreshold flickering threshold, Sabel and colleagues devised a computer-based method to map and then stimulate the border zone of visual field defects, where improvement through retraining was most likely to occur.…”