Lack of long-term cortical reorganization after macaque retinal lesions

Abstract

Several aspects of cortical organization are thought to remain plastic into adulthood, allowing cortical sensorimotor maps to be modified continuously by experience. This dynamic nature of cortical circuitry is important for learning, as well as for repair after injury to the nervous system. Electrophysiology studies suggest that adult macaque primary visual cortex (V1) undergoes large-scale reorganization within a few months after retinal lesioning, but this issue has not been conclusively settled. Here we applied the technique of functional magnetic resonance imaging (fMRI) to detect changes in the cortical topography of macaque area V1 after binocular retinal lesions. fMRI allows non-invasive, in vivo, long-term monitoring of cortical activity with a wide field of view, sampling signals from multiple neurons per unit cortical area. We show that, in contrast with previous studies, adult macaque V1 does not approach normal responsivity during 7.5 months of follow-up after retinal lesions, and its topography does not change. Electrophysiology experiments corroborated the fMRI results. This indicates that adult macaque V1 has limited potential for reorganization in the months following retinal injury.

Dynamics and specificity of cortical map reorganization after retinal lesions

“…As shown by earlier work (1-6) and the present study, topographic reorganization takes place with time in the cortical LPZ. These results have been questioned on the basis of a long-term fMRI study in monkeys that failed to reveal any recovery of the cortical hemodynamic signal (12), although multiunit recordings performed at the end of the fMRI experiments after 7.5 months showed the characteristic RF topography with ''pile-up'' of RFs and visual responses in the LPZ such as those usually seen after cortical reorganization (1)(2)(3)(4)(5)(6).…”

“…Neural responses and BOLD signal are separated in the temporal domain by an order of magnitude, and the strong early phase of multiunit activity (Ͻ2 s) in response to visual stimulation does not correlate well with the BOLD fMRI response (17). This unavoidably results in fMRI rejecting areas with shorter-lasting visual responses such as those present in the BOLDdefined LPZ center 7.5 months after retinal lesions (12). Here we have analyzed the first 1.5 s after stimulus onset, a time window that contains the most significant first 150-300 ms of neuronal information processing in the visual cortex (18,19), as well as the maximal range of late event-related computations (20).…”

“…However, cortical reorganization was questioned on the basis of the permanently reduced metabolic signal of cytochrome oxidase activity in the LPZ of primates (11). More recently, a functional MRI (fMRI) study in monkeys revealed no shrinkage of the initially silent visual cortical region [blood oxygen level-dependent (BOLD)-defined LPZ] months after retinal lesions and concluded a lack of cortical reorganization (12). Here we present details about functional recovery and the process of visuotopic reorganization in the visual cortex at the single-cell level.…”

Pulse trains to percepts: the challenge of creating a perceptually intelligible world with sight recovery technologies

“…However, in striking contrast to the literature on auditory and tactile plasticity, it is not at all clear whether the retinotopic organization of V1 is plastic in primates after infancy. A large number of studies have used either primate models [66,67] or functional magnetic resonance imaging in humans to examine how cortical retinotopic maps are affected by loss of visual input due to causes such as congenital photoreceptor abnormalities [68], chemical and thermal burns [69,70], age-related macular degeneration [71 -76] and retinitis pigmentosa [77], to list just a few. Across these many studies, there is evidence for enhanced top-down signals into deprived regions of cortex [71,73,74] even under conditions of passive viewing [74], but there is little evidence for reorganization of receptive fields within early visual areas, except in individuals where the scotoma was congenital [68].…”

Improving the performance of the amblyopic visual system

“…These studies are consistent with the notion that the connections from the amblyopic eye may be suppressed rather than destroyed. Loss of the fellow eye would allow these existing connections to be unmasked, as occurs in adult cats and monkeys with retinal lesions (Heinen & Skavenski, 1991;Chino et al 1992; but see Smirnakis et al 2005).…”