Cortical brightness adaptation when darkness and brightness produce different dynamical states in the visual cortex

Abstract

Darkness and brightness are very different perceptually. To understand the neural basis for the visual difference, we studied the dynamical states of populations of neurons in macaque primary visual cortex when a spatially uniform area (8°× 8°) of the visual field alternated between black and white. Darkness evoked sustained nerve-impulse spiking in primary visual cortex neurons, but bright stimuli evoked only a transient response. A peak in the local field potential (LFP) γ band (30-80 Hz) occurred during darkness; white-induced LFP fluctuations were of lower amplitude, peaking at 25 Hz. However, the sustained response to white in the evoked LFP was larger than for black. Together with the results on spiking, the LFP results imply that, throughout the stimulus period, bright fields evoked strong net sustained inhibition. Such cortical brightness adaptation can explain many perceptual phenomena: interocular speeding up of dark adaptation, tonic interocular suppression, and interocular masking.ight adaptation is a vitally important visual function for enabling a stable perception of the visual world when background luminance levels can be as different as night and day. Previous psychophysical studies suggested that light adaptation was caused mainly by gain control mechanisms in the retina (1-3) that have been well studied (4). However, some psychophysical results suggested that there might be also a cortical contribution to light adaptation (5), but the nature of the cortical contribution is much less well understood. Here, we report our studies of cortical adaptation to brightness and darkness in macaque primary visual cortex (V1) and the implications for visual perception.We asked the following question: how does macaque V1 cortex respond to large dark and bright regions like those that would comprise the background of a visual scene during the night or the day, respectively? The experiments reported here focused on two cortical layers, 4C and 2/3. The layers of V1 are distinct stages of processing of visual signals (6, 7). The input layer 4C is the first cortical stage where the cortex could distinguish between blackness and whiteness (8). Layer 2/3 comprise one of the main visual outputs of V1 to extrastriate visual cortex (9). To obtain a comprehensive view of the response to black and white in cortical layers 4C and 2/3, we used measurements of population activity: multiunit spike rate, termed multiunit activity (MUA), and local field potential (LFP) (10-12).Cortical brightness adaptation was evident in the qualitatively different dynamics of neural population activity in layers 4C and 2/3 when the monkeys viewed black and white regions. Both black and white large-area stimuli evoked transient excitatory responses in MUA, but in response to a white region, there was a slowly developing but much stronger inhibition of spike activity. Such suppression of sustained spiking in cortical neurons by white backgrounds would increase the signal/noise ratio of targets on white backgrounds. Such cortical brightness a...

Head Movements Control the Activity of Primary Visual Cortex in a Luminance Dependent Manner

“…Consistent with previous reports 16,17 , light itself, i.e. prior to table rotation, had an overall suppressive impact on the basal activity of V1 neurons, especially in superficial layers (Fig.…”

“…Thus, our data show that SOM cells contribute to the head movement mediated suppression of V1 neurons in the dark. Our data also demonstrate that SOM cells represent the basis for the light mediated suppression of basal activity in V1 16,17 . Importantly, RS, FS and SOM cells all showed an inverse relationship between the impact of light on basal firing rate and head-movements mediated responses: For RS and FS cells, decreasing their basal firing rate with light facilitated their response to head movements ( Fig.…”

“…Because V1 basal activity is regulated by ambient luminance [14][15][16][17] , we compared the response of V1 to head movements in dark and light conditions. To avoid contaminating V1 responses to head movements in light with responses to the visual environment, we stitched both eyelids and placed a light diffuser in front of the light source to achieve a homogeneous illumination of the eye ( Fig.…”

Functional Specialization of ON and OFF Cortical Pathways for Global-Slow and Local-Fast Vision

“…Unlike OFF spatial suppression, ON spatial suppression depends strongly on background luminance; it is nearly absent on dark backgrounds and becomes stronger than OFF spatial suppression on midgray backgrounds. The pronounced spatial suppression of light stimuli was previously demonstrated in primate visual cortex for both baseline cortical activity (Xing et al, 2014) and in response to stimuli presented on midgray backgrounds (Zurawel et al, 2014). Because midgray backgrounds make ON luminance response functions more linear, they reduce the neuronal blur of light stimuli Pons et al, 2017).…”

Effect of Age and Glaucoma on the Detection of Darks and Lights

“…4 Moreover, cortical responses to dark stimuli are stronger, faster, more linearly related to luminance contrast, and have better spatial and temporal resolution than responses to light stimuli. [5][6][7][8][9][10][11][12][13][14][15][16] Consistent with these physiological differences, dark targets are detected faster and more accurately than light targets on noisy backgrounds, 12,17 and dark pixels have a more important role in judgments of texture variance than light pixels. 18,19 Although dark/light asymmetries are most pronounced in visual cortex, 4,[6][7][8][10][11][12][13] they also are significant in the retina 9,13,[20][21][22] and possibly originate in photoreceptor outputs.…”