Aging Potentiates Lateral but Not Local Inhibition of Orientation Processing in Primary Visual Cortex

Abstract

Aging-related declines in vision can decrease well-being of the elderly. Concerning early sensory changes as in the primary visual cortex, physiological and behavioral reports seem contradictory. Neurophysiological studies on orientation tuning properties suggested that neuronal changes might come from decreased cortical local inhibition. However, behavioral results either showed no clear deficits in orientation processing in older adults, or proposed stronger surround suppression. Through psychophysical experiments and computational modeling, we resolved these discrepancies by suggesting that lateral inhibition increased in older adults while neuronal orientation tuning widths, related to local inhibition, stayed globally intact across age. We confirmed this later result by re-analyzing published neurophysiological data, which showed no systematic tuning width changes, but instead displayed a higher neuronal noise with aging. These results suggest a stronger lateral inhibition and mixed effects on local inhibition during aging, revealing a more complex picture of age-related effects in the central visual system than people previously thought.

Older Adults Exhibit Greater Visual Cortex Inhibition and Reduced Visual Cortex Plasticity Compared to Younger Adults

“…In contrast, a recent MRS study specifically targeting the primary visual cortex found significantly higher GABA levels in older (63–78 years old) relative to younger (20–34 years old) adults (Pitchaimuthu et al, 2017). This result is consistent with gene expression studies in primates (Liao et al, 2016), humans (Pinto et al, 2010), and adult primate V1 neurophysiological recordings (Wang et al, 2018), all suggesting an increase in GABA-mediated visual cortex inhibition in older relative to younger adults.…”

“…A number of psychophysical observations also provide evidence for increased GABA mediated inhibition in older adults (Karas and McKendrick, 2009, 2011, 2012; Nguyen and McKendrick, 2016; Kondo and Kochiyama, 2017; Wang et al, 2018). For example, binocular rivalry alternation rates (AR) are slower in older than in younger adults (Jalavisto, 1964; Ukai et al, 2003; Kondo and Kochiyama, 2017; Pitchaimuthu et al, 2017).…”

Differential Circuit Mechanisms of Young and Aged Visual Cortex in the Mammalian Brain

“…Even though prior reports on orientation tuning suggests that changes in neuronal response properties might result from reduced local inhibition of cortical circuits, behavioral studies in aged adults neither showed clear deficits in orientation processing nor stronger surround suppression [89]. It was also shown that lateral inhibition increases in aged adults, whereas orientation tuning widths of neurons associated to local inhibition remained globally intact with age [89]. Furthermore, there is no change in the systematic tuning width of aged adults, but instead, it showed a higher neuronal noise during aging [89].…”

“…However, different psychophysical reports on aging have shown no changes in perceptual capabilities of orientation processing leading to stronger inhibition [89]. Even though prior reports on orientation tuning suggests that changes in neuronal response properties might result from reduced local inhibition of cortical circuits, behavioral studies in aged adults neither showed clear deficits in orientation processing nor stronger surround suppression [89]. It was also shown that lateral inhibition increases in aged adults, whereas orientation tuning widths of neurons associated to local inhibition remained globally intact with age [89].…”

“…Previous reports discussing age-related neurophysiological aspects of orientation processing in animals have shown an overall decrease of inhibitory function with age and proposed that perceptual abilities in healthy aged humans might be much worse than younger adults. However, different psychophysical reports on aging have shown no changes in perceptual capabilities of orientation processing leading to stronger inhibition [89]. Even though prior reports on orientation tuning suggests that changes in neuronal response properties might result from reduced local inhibition of cortical circuits, behavioral studies in aged adults neither showed clear deficits in orientation processing nor stronger surround suppression [89].…”